Avirulent isolates of Penicillium chrysogenum to control blue mold of apple caused by P. expansum

Authors: BARTHOLOMEW, HOLLY - Oak Ridge Institute For Science And Education (ORISE); LUCIANO-ROSARIO, DIANIRIS - Oak Ridge Institute For Science And Education (ORISE); BRADSHAW, MICHAEL - Harvard University; Gaskins, Verneta; Peng, Hao; Jurick, Wayne; Fonseca, Jorge

Submitted to: Microorganisms
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 11/15/2023
Publication Date: 11/17/2023
Citation: Bartholomew, H.P., Luciano-Rosario, D., Bradshaw, M., Gaskins, V.L., Peng, H., Jurick Ii, W.M., Fonseca, J.M. 2023. Avirulent isolates of Penicillium chrysogenum to control blue mold of apple caused by P. expansum. Microorganisms. 11(11). Article e2792. https://doi.org/10.3390/microorganisms11112792.
DOI: https://doi.org/10.3390/microorganisms11112792

Interpretive Summary: Blue mold and the mycotoxins produced by the fungi that cause this disease are commonly found in stored fruit and vegetables and contribute to reductions in product quality that also incite food waste and loss. Patulin, a major mycotoxin produced by blue mold fungi, is harmful to human and animal health, and has antifungal activity. 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 strive to characterize two fungal isolates, identified as Penicillium chrysogenum, for potential use as biocontrols against blue mold and other postharvest pathogens. We demonstrate that they grow similar to blue mold pathogens, yet they create negligible harm to the apple fruit. Further, they are able to withstand the presence of patulin, indicating potential fitness when near blue mold fungi in storage, yet cannot produce it. Finally, we show these isolates reduce severity and incidence of decay when applied to wounded apple fruit prior to infection. Through these discoveries, improvements can be made to maintain fruit quality during storage and simultaneously reduce mycotoxin contamination.

Technical Abstract: Blue mold is an economically significant postharvest disease of pome fruit that is primarily caused by Penicillium expansum. To manage this disease and sustain product quality, novel decay intervention strategies are needed that also maintain long-term efficacy. Biocontrol organisms and natural products are promising tools for managing postharvest diseases. Here, two Penicillium spp. isolates, 404 and 413, were non-pathogenic in apple, yet grew rigorously in vitro when compared to the highly aggressive P. expansum R19 and Pe21 isolates. Whole genome sequencing and species-specific barcoding identified both strains as P. chrysogenum. Each P. chrysogenum strain was inoculated in apple with subsequent co-inoculation of R19 or Pe21 simultaneously, 3, or 7 days after prior inoculation with 404 or 413. Co-inoculation of these isolates showed reduced decay incidence and severity, with most significant reduction from longer establishment of P. chrysogenum. In vitro growth showed no antagonism between species, further suggesting nutrient acquisition or niche colonization as the mode of action for decay reduction. Both P. chrysogenum isolates have incomplete patulin gene clusters, yet tolerate patulin treatment. Finally, hygromycin resistance was observed for both P. chrysogenum isolates, yet they are not multi-resistant to apple postharvest fungicides. Overall, we demonstrate the translative potential of P. chrysogenum to serve as an effective biocontrol agent against blue mold decay in apples, pending practical optimization and formulation.