Omics-Based Comparison of Fungal Virulence Genes, Biosynthetic Gene Clusters, and Small Molecules in Penicillium expansum and Penicillium chrysogenum

Bartholomew, Holly P.; Gottschalk, Christopher; Cooper, Bret; Bukowski, Michael R.; Yang, Ronghui; Gaskins, Verneta L.; Luciano-Rosario, Dianiris; Fonseca, Jorge M.; Jurick, II, Wayne M.

doi:10.3390/jof11010014

Omics-Based Comparison of Fungal Virulence Genes, Biosynthetic Gene Clusters, and Small Molecules in Penicillium expansum and Penicillium chrysogenum

Journal Article · Fri Dec 27 23:00:00 EST 2024 · Journal of Fungi

DOI:https://doi.org/10.3390/jof11010014· OSTI ID:2484207

; ; Cooper, Bret; Bukowski, Michael R.; Yang, Ronghui; ; Luciano-Rosario, Dianiris; ; Jurick, II, Wayne M.

Penicillium expansum is a ubiquitous pathogenic fungus that causes blue mold decay of apple fruit postharvest, and another member of the genus, Penicillium chrysogenum, is a well-studied saprophyte valued for antibiotic and small molecule production. While these two fungi have been investigated individually, a recent discovery revealed that P. chrysogenum can block P. expansum-mediated decay of apple fruit. To shed light on this observation, we conducted a comparative genomic, transcriptomic, and metabolomic study of two P. chrysogenum (404 and 413) and two P. expansum (Pe21 and R19) isolates. Global transcriptional and metabolomic outputs were disparate between the species, nearly identical for P. chrysogenum isolates, and different between P. expansum isolates. Further, the two P. chrysogenum genomes revealed secondary metabolite gene clusters that varied widely from P. expansum. This included the absence of an intact patulin gene cluster in P. chrysogenum, which corroborates the metabolomic data regarding its inability to produce patulin. Additionally, a core subset of P. expansum virulence gene homologues were identified in P. chrysogenum and were similarly transcriptionally regulated in vitro. Molecules with varying biological activities, and phytohormone-like compounds were detected for the first time in P. expansum while antibiotics like penicillin G and other biologically active molecules were discovered in P. chrysogenum culture supernatants. Our findings provide a solid omics-based foundation of small molecule production in these two fungal species with implications in postharvest context and expand the current knowledge of the Penicillium-derived chemical repertoire for broader fundamental and practical applications.

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Sponsoring Organization:: USDOE

Grant/Contract Number:: SC0014664

OSTI ID:: 2484207

Journal Information:: Journal of Fungi, Journal Name: Journal of Fungi Journal Issue: 1 Vol. 11; ISSN 2309-608X; ISSN JFOUCU

Publisher:: MDPI AGCopyright Statement

Country of Publication:: Switzerland

Language:: English

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Identification and Functional Analysis of NLP-Encoding Genes from the Postharvest Pathogen Penicillium expansum Levin, Elena; Raphael, Ginat; Ma, Jing Microorganisms, Vol. 7, Issue 6 https://doi.org/10.3390/microorganisms7060175	journal	June 2019
Recent Advances in Phytohormone Regulation of Apple-Fruit Ripening Ji, Yinglin; Wang, Aide Plants, Vol. 10, Issue 10 https://doi.org/10.3390/plants10102061	journal	September 2021
Penicillium expansum Impact and Patulin Accumulation on Conventional and Traditional Apple Cultivars Lončarić, Ante; Šarkanj, Bojan; Gotal, Ana-Marija Toxins, Vol. 13, Issue 10 https://doi.org/10.3390/toxins13100703	journal	October 2021
Does the Host Contribute to Modulation of Mycotoxin Production by Fruit Pathogens? Kumar, Dilip; Barad, Shiri; Sionov, Edward Toxins, Vol. 9, Issue 9 https://doi.org/10.3390/toxins9090280	journal	September 2017
Whole-genome comparisons of Penicillium spp. reveals secondary metabolic gene clusters and candidate genes associated with fungal aggressiveness during apple fruit decay Wu, Guangxi; Jurick II, Wayne M.; Lichtner, Franz J. PeerJ, Vol. 7 https://doi.org/10.7717/peerj.6170	journal	January 2019

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