Comparative Penicillium spp. transcriptomics: conserved pathways and processes revealed in ungerminated conidia and during postharvest apple fruit decay

Authors: BARTHOLOMEW, HOLLY - Orise Fellow; LICHTNER, FRANZ - Orise Fellow; BRADSHAW, MICHAEL - Orise Fellow; Gaskins, Verneta; Fonseca, Jorge; BENNETT, JOAN - Rutgers University; Jurick, Wayne

Submitted to: Microorganisms
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 12/1/2022
Publication Date: 12/6/2022
Citation: Bartholomew, H.P., Lichtner, F., Bradshaw, M., Gaskins, V.L., Fonseca, J.M., Bennett, J., Jurick II, W.M. 2022. Comparative Penicillium spp. transcriptomics: conserved pathways and processes revealed in ungerminated conidia and during postharvest apple fruit decay. Microorganisms. 10(12). Article e2414. https://doi.org/10.3390/microorganisms10122414.
DOI: https://doi.org/10.3390/microorganisms10122414

Interpretive Summary: Penicillium species cause a wide variety of postharvest diseases, including blue mold decay of pome fruit. Additionally, many produce mycotoxins, which further cause rot symptoms in fruit and are harmful to humans that ingest them. To improve human health and quality of the fruit, management of blue mold disease is critical. However, traditional control methods (i.e. fungicides) are becoming less effective as resistance increases. In order to find additional infection requirements of Penicillium species during apple decay, we compared a highly virulent species with one that is much less virulent and found many novel differences between the species regarding metabolism, detoxification, and virulence strategies. We also uncovered metabolic pathways that are present in the spores of each species that could be used as targets for antifungal agents. By investigating these two pathogens, we identified a biochemical network that sustains virulence and survival requirements. Our findings can be used for abatement strategies to improve fruit quality during storage.

Technical Abstract: Blue mold, caused by Penicillium spp., is an impactful postharvest disease of pome fruit resulting in significant economic losses due to reduced fruit quality and mycotoxins. A transcriptomic approach was implemented using two Penicillium species to identify genes related to fungal aggressiveness in apple fruit and loci contained in ungerminated conidia. Total RNA was isolated from ungerminated conidia and decayed apple fruit infected with P. expansum R19 (aggressive) or P. polonicum RS1 (weak). There were 2,442 differentially expressed genes (DEGs) between the R19 and RS1 in apple and comparisons within species between apple and conidia revealed 4,404 DEGs for R19, and 2935 for RS1, respectively. Gene ontology (GO) revealed differential regulation in fungal transport and metabolism genes expressed during decay, suggesting flux in nutrient acquisition and detoxification strategies. In R19, the oxidoreductase GO category comprised 20% of all groups differentially expressed in decayed apple verses ungerminated conidia in addition to those involved in hydrogen peroxide metabolism. Ungerminated conidia from both species showed higher expression of genes encoding the glyoxylate shunt and beta-oxidation, specifying the earliest metabolic requirements for germination. This is the first study to identify and quantify pre-loaded transcripts in conidia from blue mold fungi, reveal unique genes between species expressed during apple fruit decay, and show expression dynamics of known fungal virulence factors involved in fruit decay. These findings significantly expand the fundamental knowledge base of Penicillium spp. spore germination and infection biology to enable a targeted, translational approach to develop blue mold-specific abatement strategies to maintain pome fruit quality in storage and abate mycotoxins.