Transcriptomic investigation of pyrrocidine as an inhibitor of Fusarium verticillioides growth and fumonisin production

Fusarium verticillioides and Sarocladium zeae naturally co-inhabit maize kernels and compete to maintain their ecological niches. As either an endophyte or a pathogen, F. verticillioides is a prolific fumonisin producer and a threat to food safety. As a protective endophyte of maize, S. zeae produces the antimicrobials, pyrrocidines A and B, which have been previously described to inhibit F. verticillioides fumonisin biosynthesis, and act synergistically through two pyrrocidine-induced, molecular targets – FvZBD1 (FVEG_00314) and FvABC3 (FVEG_11089) – to inhibit growth. We used transcriptomics and challenge assays coupled with analytical chemistry techniques to investigate the mechanisms of pyrrocidine-based growth and fumonisin inhibition in F. verticillioides – with the goal of preliminarily evaluating pyrrocidine as a bio-based fumonisin inhibitor for commercial maize production. Our data show that the F. verticillioides wild-type FvZBD1 rapidly transforms pyrrocidine A into pyrrocidine B, supporting the hypothesis that FvZBD1p is a core enzyme in the pyrrocidine detoxification pathway. Transcriptomic data provide evidence that pyrrocidine does not induce the expression of F. verticillioides mycotoxins or other secondary metabolites of concern. Further, we provide the first report that combined pyrrocidine A and B repress genes of the fusaric acid, bikaverin, and fusarubin biosynthetic clusters. Intriguingly, transcriptomic results also suggest that pyrrocidines may disrupt energy metabolism by shunting the tricarboxylic acid cycle and impairing the electron transport chain. This work provides promising results on pyrrocidines as fumonisin biosynthesis inhibitors and further clarifies the role of pyrrocidines and FvZBD1 in S. zeae - F. verticillioides biocontrol interactions.