Abstract
The ubiquitous ascomycete Fusarium verticillioides causes ear rot and stalk rot of maize, both of which reduce grain quality and yield. Additionally, F. verticillioides produces the mycotoxin fumonisin B1 (FB1) during infection of maize kernels, and thus potentially compromises human and animal health. The current knowledge is fragmentary regarding the regulation of FB1 biosynthesis, particularly when considering interplay with environmental factors such as nutrient availability. In this study, SDA1 of F. verticillioides, predicted to encode a Cys-2 His-2 zinc finger transcription factor, was shown to play a key role in catabolizing select carbon sources. Growth of the SDA1 knock-out mutant (Δsda1) was completely inhibited when sorbitol was the sole carbon source and was severely impaired when exclusively provided mannitol or glycerol. Deletion of SDA1 unexpectedly increased FB1 biosynthesis, but reduced arabitol and mannitol biosynthesis, as compared to the wild-type progenitor. Trichoderma reesei ACE1, a regulator of cellulase and xylanase expression, complemented the F. verticillioides Δsda1 mutant, which indicates that Ace1 and Sda1 are functional orthologs. Taken together, the data indicate that Sda1 is a transcriptional regulator of carbon metabolism and toxin production in F. verticillioides.
Highlights
In nature, fungi utilize a broad range of carbon sources for anabolism and energy [1]
A limited number of zinc finger transcription factor (TF) are known to regulate the expression of F. verticillioides FUM genes, which directly influences fumonisin B1 (FB1) biosynthesis [23,28,57,58]
The Cys-2 His-2 (C2H2) TF Pac1 is an ortholog of A. nidulans pacC, which is a transcriptional regulator of pH-responsive pathways
Summary
Fungi utilize a broad range of carbon sources for anabolism and energy [1]. Extensive efforts have elucidated carbon metabolic pathways in Saccharomyces cerevisiae that are broadly conserved among yeast species [2]. S. cerevisiae and many other yeasts utilize mono and disaccharides through conserved metabolic networks such as glycolysis, the tricarboxylic acid cycle, and the pentose phosphate pathway [1]. S. cerevisiae does not possess some of the more complex sugar metabolic pathways found in filamentous fungi, such as for the biosynthesis of polyols (sugar alcohols). Filamentous fungi produce a wide range of polyols, including mannitol, which is one of the most common polyols found in nature [4,5]. Polyol biosynthesis can be activated by the presence of high glucose levels [10], where glucose is reduced to sorbitol by aldose reductase (AR), and subsequently oxidized to fructose by sorbitol dehydrogenase (SDH). A clear fungal ortholog of mammalian SDH is not known to exist [12]
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