A Novel Population of Fusarium fujikuroi Isolated from Southeastern U.S. Winegrapes Reveals the Need to Re-Evaluate the Species’ Fumonisin Production

Abstract

Mycotoxins pose a challenge to a safe food supply worldwide, and their threat is expected to worsen with our changing climate. The need for diligence is exemplified by the discovery of fumonisin B2 in wine, which joins ochratoxin A as a mycotoxin of concern in the grape-wine chain. To elucidate the mycotoxin risk in southeastern American wine, grape samples were collected from vineyards during harvest in 2013 and potentially mycotoxigenic fungi (Fusarium and Aspergillus) were isolated from the samples. Numerous Fusarium isolates were recovered and identified to the species level by comparison of translation elongation factor 1-α gene sequences to verified strains. Fusarium fujikuroi was the most abundant species recovered (239 isolates), followed by F. proliferatum (52), F. incarnatum-equiseti (14), F. oxysporum (7), F. concentricum (1), and F. solani (1). In vitro assays quantified fumonisin production for representative isolates via liquid chromatography-tandem mass spectrometry. Surprisingly, nearly all F. fujikuroi isolates produced fumonisins B1, B2, and B3 at levels comparable to both the F. proliferatum isolates and the positive control, Fusarium verticillioides. Such capacity for fumonisin production refutes the generally accepted notion that F. fujikuroi produces undetectable or low levels of fumonisins and provides evidence to reconsider this species as a mycotoxigenic threat to economically significant crops.

Endohyphal bacteria associated with virulence, increased expression of fumonisin biosynthetic genes, and production of fumonisin and macroconidia in Fusarium fujikuroi W343

“…Production of FB 1 , FB 2 and FB 3 by Ffuji was detected under fumonisin‐inducing experimental conditions in this study. This finding is consistent with recent reports of fumonisin production by other isolates of F. fujikuroi (Matić et al , ; Bolton et al , ). Fumonisin production and increased expression of four fumonisin biosynthetic genes by the fungus, under the fumonisin‐inducing conditions, were also observed to correlate with the presence of endohyphal bacteria.…”

“…Ffuji, cured‐Ffuji, restored‐Ffuji‐En1, restored‐Ffuji‐En2 and restored‐Ffuji‐En1‐2 were assayed for fumonisin production as previously described by Bolton et al (), with slight modifications. Five millilitres of filter‐sterilized autoclaved distilled water was added to 3 g rice (parboiled enriched long grain rice; Member’s Mark) in 20 mL scintillation vials and topped with cotton plugs.…”

“…Members of the Gibberella fujikuroi species complex (GFSC) include more than 45 phylogenetic species, 10 biological and morphological species, 34 morphospecies (Moussa et al , ), and more than nine mating populations (Leslie & Summerell, ). Fusarium fujikuroi , which belongs to mating population C (MP‐C) (Leslie & Summerell, ), infects and causes disease in several crops including ear and root rot of corn (Leyva‐Madrigal et al , ), bakanae or foolish seedling disease in rice (Desjardins et al , ; Carter et al , ) and grapevine (Bolton et al , ).…”

“…Fumonisins, a group of polyketide‐derived mycotoxins, are produced by members of the GFSC including F. fujikuroi , F. verticillioides (teleomorph G. moniliformis ) and F. proliferatum (teleomorph G. intermedia ) (Matić et al , ; Bolton et al , ). Fumonisins comprise three groups, namely A, B and C (Powell & Plattner, ).…”

“…Fusarium fujikuroi was widely described as a non‐producer, producing little to no B‐fumonisins despite having a complement of fumonisin biosynthetic genes comparable to those present in F. verticillioides and F. proliferatum (Wiemann et al , ). However, in a recent report, strains of F. fujikuroi isolated from southeastern US grapevines were shown to produce fumonisins B 1 , B 2 and B 3 at levels comparable to those of F. verticillioides and F. proliferatum (Bolton et al , ), necessitating a need to reevaluate the characterization of F. fujikuroi as a relatively weak to non‐producer of fumonisins.…”