Fumonisin and Beauvericin Chemotypes and Genotypes of the Sister Species Fusarium subglutinans and Fusarium temperatum

Abstract

Fusarium subglutinans and Fusarium temperatum are common maize pathogens that produce mycotoxins and cause plant disease. The ability of these species to produce beauvericin and fumonisin mycotoxins is not settled, as reports of toxin production are not concordant. Our objective was to clarify this situation by determining both the chemotypes and genotypes for strains from both species. We analyzed 25 strains from Argentina, 13 F. subglutinans and 12 F. temperatum strains, for toxin production by ultraperformance liquid chromatography mass spectrometry (UPLC-MS). We used new genome sequences from two strains of F. subglutinans and one strain of F. temperatum, plus genomes of other Fusarium species, to determine the presence of functional gene clusters for the synthesis of these toxins. None of the strains examined from either species produced fumonisins. These strains also lack Fum biosynthetic genes but retain homologs of some genes that flank the Fum cluster in Fusarium verticillioides. None of the F. subglutinans strains we examined produced beauvericin although 9 of 12 F. temperatum strains did. A complete beauvericin (Bea) gene cluster was present in all three new genome sequences. The Bea1 gene was presumably functional in F. temperatum but was not functional in F. subglutinans due to a large insertion and multiple mutations that resulted in premature stop codons. The accumulation of only a few mutations expected to disrupt Bea1 suggests that the process of its inactivation is relatively recent. Thus, none of the strains of F. subglutinans or F. temperatum we examined produce fumonisins, and the strains of F. subglutinans examined also cannot produce beauvericin. Variation in the ability of strains of F. temperatum to produce beauvericin requires further study and could reflect the recent shared ancestry of these two species. IMPORTANCE Fusarium subglutinans and F. temperatum are sister species and maize pathogens commonly isolated worldwide that can produce several mycotoxins and cause seedling disease, stalk rot, and ear rot. The ability of these species to produce beauvericin and fumonisin mycotoxins is not settled, as reports of toxin production are not concordant at the species level. Our results are consistent with previous reports that strains of F. subglutinans produce neither fumonisins nor beauvericin. The status of toxin production by F. temperatum needs further work. Our strains of F. temperatum did not produce fumonisins, while some strains produced beauvericin and others did not. These results enable more accurate risk assessments of potential mycotoxin contamination if strains of these species are present. The nature of the genetic inactivation of BEA1 is consistent with its relatively recent occurrence and the close phylogenetic relationship of the two sister species.

Natural Occurrence of Mycotoxin-Producing Fusaria in Market-Bought Peruvian Cereals: A Food Safety Threat for Andean Populations

“…In their previous assessment in Peru, Logrieco and colleagues found the strains of F. subglutinans they isolated to primarily produce beauvericin and moniliformin, two mycotoxins qualified as “emerging”, i.e., mycotoxins that are “neither routinely determined, nor legislatively regulated” with, however, “the evidence of their incidence is rapidly increasing” [ 43 ]. In line with these results, in Argentina, F. temperatum was also detected as a frequent contaminant of maize kernels but isolated strains largely produced beauvericin and only a few of them produced Fumonisins [ 44 , 45 ]. Consistent monitoring across several years would be required considering that Peru is subjected to extreme climatic events, notably El Niño/La Niña events, that are prime factors for contaminations with mycotoxins [ 46 ].…”

Occurrence, Pathogenicity, and Mycotoxin Production of Fusarium temperatum in Relation to Other Fusarium Species on Maize in Germany

“…FB1 and FB2 were also detected in one culture of F. subglutinans. Even though F. subglutinans was occasionally reported to produce fumonisins [ 63 ], which is a common feature among members of the FFSC, both classical [ 18 ] as well as modern studies [ 64 , 65 , 66 , 67 ] convincingly showed that F. subglutinans does not produce fumonisins. Mycotoxin production found in a small set of cultures of F. verticillioides and F. proliferatum confirmed the established mycotoxin spectra of these species [ 59 , 68 , 69 , 70 ].…”

Genetic Background of Variable Fumonisin Production in the <i>Fusarium Fujikuroi</i> Species Complex

“…In the FFSC, the ability of fumonisin production is correlated with the presence of FUM genes but not correlated with phylogenetic relationships [59,87]. Lack of FUM genes was indicated in the species that had been reported as fumonisin producer (F. napiforme, F. dlamni, F. subglutinans, F. temperatum) [67,77,89,90]. The possible reason for these irrationals is an intraspecific variation of fumonisin producibility.…”

“…Wang et al [75] reported that F. temperatum from maize in China produced fumonisin under field conditions and Fumero et al [76] detected fumonisin production in 25% of F. temperatum strains from maize in Argentina. Recently, Fumero et al [77] obtained the whole genome sequence of a F. subglutinans strain and a F. temperatum strain from Argentina and that suggested absence of FUM genes and fumonisin production in these strains.…”