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4-O-Glucosylation of Trichothecenes by Fusarium Species: A Phase II Xenobiotic Metabolism for t-Type Trichothecene Producers.

ABSTRACT: The t-type trichothecene producers Fusarium sporotrichioides and Fusarium graminearum protect themselves against their own mycotoxins by acetylating the C-3 hydroxy group with Tri101p acetylase. To understand the mechanism by which they deal with exogenously added d-type trichothecenes, the Δtri5 mutants expressing all but the first trichothecene pathway enzymes were fed with trichodermol (TDmol), trichothecolone (TCC), 8-deoxytrichothecin, and trichothecin. LC-MS/MS and NMR analyses showed that these C-3 unoxygenated trichothecenes were conjugated with glucose at C-4 by α-glucosidic linkage. As t-type trichothecenes are readily incorporated into the biosynthetic pathway following the C-3 acetylation, the mycotoxins were fed to the ΔFgtri5ΔFgtri101 mutant to examine their fate. LC-MS/MS and NMR analyses demonstrated that the mutant conjugated glucose at C-4 of HT-2 toxin (HT-2) by α-glucosidic linkage, while the ΔFgtri5 mutant metabolized HT-2 to 3-acetyl HT-2 toxin and T-2 toxin. The 4-O-glucosylation of exogenously added t-type trichothecenes appears to be a general response of the ΔFgtri5ΔFgtri101 mutant, as nivalenol and its acetylated derivatives appeared to be conjugated with hexose to some extent. The toxicities of 4-O-glucosides of TDmol, TCC, and HT-2 were much weaker than their corresponding aglycons, suggesting that 4-O-glucosylation serves as a phase II xenobiotic metabolism for t-type trichothecene producers.

SUBMITTER: Matsui K

PROVIDER: S-EPMC8709292 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:The Fusarium sambucinum species complex (FSAMSC) is one of the most taxonomically challenging groups of fusaria, comprising prominent mycotoxigenic plant pathogens and other species with various lifestyles. Among toxins produced by members of the FSAMSC, trichothecenes pose the most significant threat to public health. Herein a global collection of 171 strains, originating from diverse hosts or substrates, were selected to represent FSAMSC diversity. This strain collection was used to assess their species diversity, evaluate their potential to produce trichothecenes, and cause disease on wheat. Maximum likelihood and Bayesian analyses of a combined 3-gene dataset used to infer evolutionary relationships revealed that the 171 strains originally received as 48 species represent 74 genealogically exclusive phylogenetically distinct species distributed among six strongly supported clades: Brachygibbosum, Graminearum, Longipes, Novel, Sambucinum, and Sporotrichioides. Most of the strains produced trichothecenes in vitro but varied in type, indicating that the six clades correspond to type A, type B, or both types of trichothecene-producing lineages. Furthermore, five strains representing two putative novel species within the Sambucinum Clade produced two newly discovered type A trichothecenes, 15-keto NX-2 and 15-keto NX-3. Strains of the two putatively novel species together with members of the Graminearum Clade were aggressive toward wheat when tested for pathogenicity on heads of the susceptible cultivar Apogee. In planta, the Graminearum Clade strains produced nivalenol or deoxynivalenol and the aggressive Sambucinum Clade strains synthesized NX-3 and 15-keto NX-3. Other strains within the Brachygibbosum, Longipes, Novel, Sambucinum, and Sporotrichioides Clades were nonpathogenic or could infect the inoculated floret without spreading within the head. Moreover, most of these strains did not produce any toxin in the inoculated spikelets. These data highlight aggressiveness toward wheat appears to be influenced by the type of toxin produced and that it is not limited to members of the Graminearum Clade.

Project description:BackgroundFusarium head blight (FHB) of wheat caused by Fusarium graminearum species complex (FGSC) is a devastating disease worldwide. The pathogens not only reduce the yield of wheat, but also impact the quality of wheat by contamination with trichothecene mycotoxins. A systematic investigation on the pathogens of FHB in Taiwan is lacking. Here, molecular and morphological approaches were used to identify species of the Taiwanese FGSC isolates and determine their trichothecene genotypes.ResultsIn this study, a total of 195 isolates of FGSC from diseased wheat were collected from 8 areas of northern and central Taiwan. All isolates were subjected to seedling inoculation for verification of pathogenicity. The pathogenic isolates were genetically characterized by sequence characterized amplified region (SCAR), PCR- restriction fragment length polymorphism (RFLP), phylogenetic analysis and fixed nucleotides to clarify their phylogenetic species, and by PCR assays of TRI genes to determine trichothecene genotypes. They were identified as F. asiaticum, F. graminearum sensu stricto, F. meridionale and an unknown species. Isolates of F. asiaticum were the major causal agents (98%) in this investigated population and were comprised of SCAR type 5 (75%), SCAR type 4 (21%) and SCAR type 3 (2%). Their trichothecene genotypes were either 15-acetyl-deoxynivalenol (15-ADON) (83%) or nivalenol (NIV) genotype (17%). These genetic characterizations indicated that F. asiaticum (15-ADON SCAR type 5) accounts for 60% of this Taiwanese population. Virulence assay on wheat heads indicated virulence of F. asiaticum isolates in subpopulations divided by SCAR types or trichothecene genotypes were comparable, suggesting other factors influence the unequal subpopulation sizes.ConclusionsThis is the first study that FGSC isolates in Taiwan were systematically collected and characterized. In addition to F. graminearum sensu stricto and F. meridionale, F. asiaticum with 15-ADON genotype was identified as the predominate species in Taiwan. In contrast to Chinese and Japanese populations that F. asiaticum isolates were typically of 3-ADON or NIV genotype, the predominate 15-ADON genotype in Taiwanese population was unique among F. asiaticum populations and represented the southernmost 15-ADON genotype population in East Asia.

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4-O-Glucosylation of Trichothecenes by Fusarium Species: A Phase II Xenobiotic Metabolism for t-Type Trichothecene Producers.

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