More than just a virulence factor: patulin is a non-host specific toxin requiring active efflux for auto-avoidance in Penicillium spp. and inhibits growth of multiple postharvest fungal pathogens

Authors: BARTHOLOMEW, HOLLY - Oak Ridge Institute For Science And Education (ORISE); BRADSHAW, MICHAEL - Oak Ridge Institute For Science And Education (ORISE); Macarisin, Otilia; Gaskins, Verneta; Fonseca, Jorge; Jurick, Wayne

Submitted to: Toxins
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 11/4/2021
Publication Date: 4/2/2022
Citation: Bartholomew, H.P., Bradshaw, M., Macarisin, O., Gaskins, V.L., Fonseca, J.M., Jurick II, W.M. 2022. More than just a virulence factor: patulin is a non-host specific toxin requiring active efflux for auto-avoidance in Penicillium spp. and inhibits growth of multiple postharvest fungal pathogens. Toxins. 112:1165-1174. https://doi.org/10.1094/PHYTO-09-21-0371-R.
DOI: https://doi.org/10.1094/PHYTO-09-21-0371-R

Interpretive Summary: Mycotoxins are commonly found in stored fruit and vegetables and contribute to reductions in product quality that also incite food waste and loss. Patulin, the focal mycotoxin of this manuscript, is harmful to human and animal health, and this study reveals that it causes harm to apple fruit even in the absence of the fungi that produce it. Therefore, it is clear this mycotoxin harms not just humans, but also their fruit host. Further investigation examined the impact patulin has on other fungi and other fruit. As conventional methods of decay control (e.g. fungicides) are being reduced, alternatives are being sought to reduce food waste from mycotoxin producing fungi. The current efforts have uncovered the susceptibility of various organisms to patulin and the mode of action of the mycotoxin. These works have uncovered a novel mechanism through which some fungi are capable of patulin tolerance. Through these discoveries, improvements in toxin abatement and disease control can be made to maintain fruit quality during storage and simultaneously reduce mycotoxin contamination.

Technical Abstract: Mycotoxin contamination is a leading cause of food spoilage and waste on a global scale. Patulin, a mycotoxin produced by Penicillium spp. during postharvest pome fruit decay, causes acute and chronic effects in humans, withstands pasteurization, and is not eliminated during fermentation. While much is known about the impact of patulin on human health, there are significant knowledge gaps concerning the effect of patulin on postharvest fruit-pathogen- interactions. Inoculation of six apple cultivars with patulin recreated some of the blue mold symptoms which were cultivar-independent and dose-dependent. Identical symptoms were also observed in pear and mandarin, revealing broad range, non-host specificity. Six Penicillium isolates exposed to exogenous patulin exhibited delayed germination, yet all produced viable colonies over time. However, four common postharvest phytopathogenic fungi were completely inhibited in germination and growth, suggesting patulin is important to allow Penicillium to dominate the postharvest fruit niche. Using clorgyline, an efflux pump inhibitor, we demonstrated that active efflux plays a pivotal role in Penicillium auto-resistance to patulin during conidial germination. The work presented here contributes new knowledge of patulin auto-resistance, its mode of action, and inhibitory role in fungal-fungal interactions. Our findings provide a solid foundation to develop toxin and decay mitigation approaches.