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

<i>Penicillium expansum</i> is a ubiquitous pathogenic fungus that causes blue mold decay of apple fruit postharvest, and another member of the genus, <i>Penicillium chrysogenum</i>, is a well-studied saprophyte valued for antibiotic and small molecule production. While these...

Full description

Saved in:
Bibliographic Details
Main Authors: Holly P. Bartholomew, Christopher Gottschalk, Bret Cooper, Michael R. Bukowski, Ronghui Yang, Verneta L. Gaskins, Dianiris Luciano-Rosario, Jorge M. Fonseca, Wayne M. Jurick
Format: Article
Language:English
Published: MDPI AG 2024-12-01
Series:Journal of Fungi
Subjects:
Online Access:https://www.mdpi.com/2309-608X/11/1/14
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1832588206992785408
author Holly P. Bartholomew
Christopher Gottschalk
Bret Cooper
Michael R. Bukowski
Ronghui Yang
Verneta L. Gaskins
Dianiris Luciano-Rosario
Jorge M. Fonseca
Wayne M. Jurick
author_facet Holly P. Bartholomew
Christopher Gottschalk
Bret Cooper
Michael R. Bukowski
Ronghui Yang
Verneta L. Gaskins
Dianiris Luciano-Rosario
Jorge M. Fonseca
Wayne M. Jurick
author_sort Holly P. Bartholomew
collection DOAJ
description <i>Penicillium expansum</i> is a ubiquitous pathogenic fungus that causes blue mold decay of apple fruit postharvest, and another member of the genus, <i>Penicillium chrysogenum</i>, 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 <i>P. chrysogenum</i> can block <i>P. expansum-</i>mediated decay of apple fruit. To shed light on this observation, we conducted a comparative genomic, transcriptomic, and metabolomic study of two <i>P. chrysogenum</i> (404 and 413) and two <i>P. expansum</i> (Pe21 and R19) isolates. Global transcriptional and metabolomic outputs were disparate between the species, nearly identical for <i>P. chrysogenum</i> isolates, and different between <i>P. expansum</i> isolates. Further, the two <i>P. chrysogenum</i> genomes revealed secondary metabolite gene clusters that varied widely from <i>P. expansum</i>. This included the absence of an intact patulin gene cluster in <i>P. chrysogenum</i>, which corroborates the metabolomic data regarding its inability to produce patulin. Additionally, a core subset of <i>P. expansum</i> virulence gene homologues were identified in <i>P. chrysogenum</i> and were similarly transcriptionally regulated in vitro. Molecules with varying biological activities, and phytohormone-like compounds were detected for the first time in <i>P. expansum</i> while antibiotics like penicillin G and other biologically active molecules were discovered in <i>P. chrysogenum</i> 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 <i>Penicillium</i>-derived chemical repertoire for broader fundamental and practical applications.
format Article
id doaj-art-6fb875e83a7a45918170ee0edfbc69a3
institution Kabale University
issn 2309-608X
language English
publishDate 2024-12-01
publisher MDPI AG
record_format Article
series Journal of Fungi
spelling doaj-art-6fb875e83a7a45918170ee0edfbc69a32025-01-24T13:37:13ZengMDPI AGJournal of Fungi2309-608X2024-12-011111410.3390/jof11010014Omics-Based Comparison of Fungal Virulence Genes, Biosynthetic Gene Clusters, and Small Molecules in <i>Penicillium expansum</i> and <i>Penicillium chrysogenum</i>Holly P. Bartholomew0Christopher Gottschalk1Bret Cooper2Michael R. Bukowski3Ronghui Yang4Verneta L. Gaskins5Dianiris Luciano-Rosario6Jorge M. Fonseca7Wayne M. Jurick8Food Quality Laboratory, U.S. Department of Agriculture, Agricultural Research Service, Beltsville Agricultural Research Center, Beltsville, MD 20705, USAInnovative Fruit Production, Improvement, and Protection, Appalachian Fruit Research Station, U.S. Department of Agriculture, Agricultural Research Service, Kearneysville, WV 25430, USASoybean Genomics and Improvement Laboratory, U.S. Department of Agriculture, Agricultural Research Service, Beltsville Agricultural Research Center, Beltsville, MD 20705, USAMethods and Application of Food Composition Laboratory, U.S. Department of Agriculture, Agricultural Research Service, Beltsville Human Nutrition Research Center, Beltsville, MD 20705, USASoybean Genomics and Improvement Laboratory, U.S. Department of Agriculture, Agricultural Research Service, Beltsville Agricultural Research Center, Beltsville, MD 20705, USAFood Quality Laboratory, U.S. Department of Agriculture, Agricultural Research Service, Beltsville Agricultural Research Center, Beltsville, MD 20705, USAFood Quality Laboratory, U.S. Department of Agriculture, Agricultural Research Service, Beltsville Agricultural Research Center, Beltsville, MD 20705, USAFood Quality Laboratory, U.S. Department of Agriculture, Agricultural Research Service, Beltsville Agricultural Research Center, Beltsville, MD 20705, USAFood Quality Laboratory, U.S. Department of Agriculture, Agricultural Research Service, Beltsville Agricultural Research Center, Beltsville, MD 20705, USA<i>Penicillium expansum</i> is a ubiquitous pathogenic fungus that causes blue mold decay of apple fruit postharvest, and another member of the genus, <i>Penicillium chrysogenum</i>, 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 <i>P. chrysogenum</i> can block <i>P. expansum-</i>mediated decay of apple fruit. To shed light on this observation, we conducted a comparative genomic, transcriptomic, and metabolomic study of two <i>P. chrysogenum</i> (404 and 413) and two <i>P. expansum</i> (Pe21 and R19) isolates. Global transcriptional and metabolomic outputs were disparate between the species, nearly identical for <i>P. chrysogenum</i> isolates, and different between <i>P. expansum</i> isolates. Further, the two <i>P. chrysogenum</i> genomes revealed secondary metabolite gene clusters that varied widely from <i>P. expansum</i>. This included the absence of an intact patulin gene cluster in <i>P. chrysogenum</i>, which corroborates the metabolomic data regarding its inability to produce patulin. Additionally, a core subset of <i>P. expansum</i> virulence gene homologues were identified in <i>P. chrysogenum</i> and were similarly transcriptionally regulated in vitro. Molecules with varying biological activities, and phytohormone-like compounds were detected for the first time in <i>P. expansum</i> while antibiotics like penicillin G and other biologically active molecules were discovered in <i>P. chrysogenum</i> 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 <i>Penicillium</i>-derived chemical repertoire for broader fundamental and practical applications.https://www.mdpi.com/2309-608X/11/1/14appleblue mold<i>Penicillium expansum</i><i>Penicillium chrysogenum</i>metabolomicssecondary metabolites
spellingShingle Holly P. Bartholomew
Christopher Gottschalk
Bret Cooper
Michael R. Bukowski
Ronghui Yang
Verneta L. Gaskins
Dianiris Luciano-Rosario
Jorge M. Fonseca
Wayne M. Jurick
Omics-Based Comparison of Fungal Virulence Genes, Biosynthetic Gene Clusters, and Small Molecules in <i>Penicillium expansum</i> and <i>Penicillium chrysogenum</i>
Journal of Fungi
apple
blue mold
<i>Penicillium expansum</i>
<i>Penicillium chrysogenum</i>
metabolomics
secondary metabolites
title Omics-Based Comparison of Fungal Virulence Genes, Biosynthetic Gene Clusters, and Small Molecules in <i>Penicillium expansum</i> and <i>Penicillium chrysogenum</i>
title_full Omics-Based Comparison of Fungal Virulence Genes, Biosynthetic Gene Clusters, and Small Molecules in <i>Penicillium expansum</i> and <i>Penicillium chrysogenum</i>
title_fullStr Omics-Based Comparison of Fungal Virulence Genes, Biosynthetic Gene Clusters, and Small Molecules in <i>Penicillium expansum</i> and <i>Penicillium chrysogenum</i>
title_full_unstemmed Omics-Based Comparison of Fungal Virulence Genes, Biosynthetic Gene Clusters, and Small Molecules in <i>Penicillium expansum</i> and <i>Penicillium chrysogenum</i>
title_short Omics-Based Comparison of Fungal Virulence Genes, Biosynthetic Gene Clusters, and Small Molecules in <i>Penicillium expansum</i> and <i>Penicillium chrysogenum</i>
title_sort omics based comparison of fungal virulence genes biosynthetic gene clusters and small molecules in i penicillium expansum i and i penicillium chrysogenum i
topic apple
blue mold
<i>Penicillium expansum</i>
<i>Penicillium chrysogenum</i>
metabolomics
secondary metabolites
url https://www.mdpi.com/2309-608X/11/1/14
work_keys_str_mv AT hollypbartholomew omicsbasedcomparisonoffungalvirulencegenesbiosyntheticgeneclustersandsmallmoleculesinipenicilliumexpansumiandipenicilliumchrysogenumi
AT christophergottschalk omicsbasedcomparisonoffungalvirulencegenesbiosyntheticgeneclustersandsmallmoleculesinipenicilliumexpansumiandipenicilliumchrysogenumi
AT bretcooper omicsbasedcomparisonoffungalvirulencegenesbiosyntheticgeneclustersandsmallmoleculesinipenicilliumexpansumiandipenicilliumchrysogenumi
AT michaelrbukowski omicsbasedcomparisonoffungalvirulencegenesbiosyntheticgeneclustersandsmallmoleculesinipenicilliumexpansumiandipenicilliumchrysogenumi
AT ronghuiyang omicsbasedcomparisonoffungalvirulencegenesbiosyntheticgeneclustersandsmallmoleculesinipenicilliumexpansumiandipenicilliumchrysogenumi
AT vernetalgaskins omicsbasedcomparisonoffungalvirulencegenesbiosyntheticgeneclustersandsmallmoleculesinipenicilliumexpansumiandipenicilliumchrysogenumi
AT dianirislucianorosario omicsbasedcomparisonoffungalvirulencegenesbiosyntheticgeneclustersandsmallmoleculesinipenicilliumexpansumiandipenicilliumchrysogenumi
AT jorgemfonseca omicsbasedcomparisonoffungalvirulencegenesbiosyntheticgeneclustersandsmallmoleculesinipenicilliumexpansumiandipenicilliumchrysogenumi
AT waynemjurick omicsbasedcomparisonoffungalvirulencegenesbiosyntheticgeneclustersandsmallmoleculesinipenicilliumexpansumiandipenicilliumchrysogenumi