The Near-Gapless Penicillium fuscoglaucum Genome Enables the Discovery of Lifestyle Features as an Emerging Post-Harvest Phytopathogen

Luciano-Rosario, Dianiris; Jurick, Wayne M.; Gottschalk, Christopher

doi:10.3390/jof10060430

Title: The Near-Gapless Penicillium fuscoglaucum Genome Enables the Discovery of Lifestyle Features as an Emerging Post-Harvest Phytopathogen

Journal Article · Tue Jun 18 00:00:00 UTC 2024 · Journal of Fungi

DOI: https://doi.org/10.3390/jof10060430 · OSTI ID:2469765

Luciano-Rosario, Dianiris ^[1]; Jurick, Wayne M. ^[2];

^[3]

USDA-ARS, Beltsville, MD (United States); ORISE Postdoctoral Research Fellow, Oak Ridge, TN (United States)
USDA-ARS, Beltsville, MD (United States)
USDA-ARS, Kearneysville, WV (United States)

Penicillium spp. occupy many diverse biological niches that include plant pathogens, opportunistic human pathogens, saprophytes, indoor air contaminants, and those selected specifically for industrial applications to produce secondary metabolites and lifesaving antibiotics. Recent phylogenetic studies have established Penicillium fuscoglaucum as a synonym for Penicillium commune, which is an indoor air contaminant and toxin producer and can infect apple fruit during storage. During routine culturing on selective media in the lab, we obtained an isolate of P. fuscoglaucum Pf_T2 and sequenced its genome. The Pf_T2 genome is far superior to available genomic resources for the species. Our assembly exhibits a length of 35.1 Mb, a BUSCO score of 97.9% complete, and consists of five scaffolds/contigs representing the four expected chromosomes. It was determined that the Pf_T2 genome was colinear with a type specimen P. fuscoglaucum and contained a lineage-specific, intact cyclopiazonic acid (CPA) gene cluster. For comparison, a highly virulent postharvest apple pathogen, P. expansum strain TDL 12.1, was included and showed a similar growth pattern in culture to our Pf_T2 isolate but was far more aggressive in apple fruit than P. fuscoglaucum. The genome of Pf_T2 serves as a major improvement over existing resources, has superior annotation, and can inform forthcoming omics-based work and functional genetic studies to probe secondary metabolite production and disparities in aggressiveness during apple fruit decay.

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Research Organization:: Oak Ridge Institute for Science and Education (ORISE), Oak Ridge, TN (United States)

Sponsoring Organization:: USDA; USDOE Office of Science (SC)

Grant/Contract Number:: SC0014664

OSTI ID:: 2469765

Journal Information:: Journal of Fungi, Journal Name: Journal of Fungi Journal Issue: 6 Vol. 10; ISSN 2309-608X

Publisher:: MDPICopyright Statement

Country of Publication:: United States

Language:: English

References (41)

Fast and Easy Method for Construction of Plasmid Vectors Using Modified Quick-Change Mutagenesis Bok, Jin Woo; Keller, Nancy P. Methods in Molecular Biology https://doi.org/10.1007/978-1-62703-122-6_11	book	January 2012
Chemical profile of the secondary metabolites produced by a deep-sea sediment-derived fungus Penicillium commune SD-118 Shang, Zhuo; Li, Xiaoming; Meng, Li Chinese Journal of Oceanology and Limnology, Vol. 30, Issue 2 https://doi.org/10.1007/s00343-012-1075-1	journal	March 2012
Penicillium commune, P. camembertii, the origin of white cheese moulds, and the production of cyclopiazonic acid Pitt, J. I.; Cruickshank, R. H.; Leistner, L. Food Microbiology, Vol. 3, Issue 4 https://doi.org/10.1016/0740-0020(86)90022-5	journal	October 1986
Distribution of Penicillium commune isolates in cheese dairies mapped using secondary metabolite profiles, morphotypes, RAPD and AFLP fingerprinting Lund, Flemming; Nielsen, Anni Bech; Skouboe, Pernille Food Microbiology, Vol. 20, Issue 6 https://doi.org/10.1016/S0740-0020(02)00160-0	journal	December 2003
Adaptive Horizontal Gene Transfers between Multiple Cheese-Associated Fungi Ropars, Jeanne; Rodríguez de la Vega, Ricardo C.; López-Villavicencio, Manuela Current Biology, Vol. 25, Issue 19 https://doi.org/10.1016/j.cub.2015.08.025	journal	October 2015
Domestication of the Emblematic White Cheese-Making Fungus Penicillium camemberti and Its Diversification into Two Varieties Ropars, Jeanne; Didiot, Estelle; Rodríguez de la Vega, Ricardo C. Current Biology, Vol. 30, Issue 22 https://doi.org/10.1016/j.cub.2020.08.082	journal	November 2020
The role and fate of patulin in apple-associated fungal-fungal interactions Clemmensen, Sidsel Ettrup; Cowled, Michael Scott; Kromphardt, Kresten Jon Korup Fungal Ecology, Vol. 69 https://doi.org/10.1016/j.funeco.2024.101341	journal	June 2024
Citrinin as an accessory establishment factor of P. expansum for the colonization of apples Touhami, Najim; Soukup, Sebastian T.; Schmidt-Heydt, Markus International Journal of Food Microbiology, Vol. 266 https://doi.org/10.1016/j.ijfoodmicro.2017.12.007	journal	February 2018
Classification of Aspergillus, Penicillium, Talaromyces and related genera (Eurotiales): An overview of families, genera, subgenera, sections, series and species Houbraken, J.; Kocsubé, S.; Visagie, C. M. Studies in Mycology, Vol. 95 https://doi.org/10.1016/j.simyco.2020.05.002	journal	March 2020
Characterization and Biosynthesis of a Rare Fungal Hopane-Type Triterpenoid Glycoside Involved in the Antistress Property of Aspergillus fumigatus Ma, Ke; Zhang, Peng; Tao, Qiaoqiao Organic Letters, Vol. 21, Issue 9 https://doi.org/10.1021/acs.orglett.9b00984	journal	April 2019
Penicillium expansum : Consistent Production of Patulin, Chaetoglobosins, and Other Secondary Metabolites in Culture and Their Natural Occurrence in Fruit Products Andersen, Birgitte; Smedsgaard, Jørn; Frisvad, Jens C. Journal of Agricultural and Food Chemistry, Vol. 52, Issue 8 https://doi.org/10.1021/jf035406k	journal	April 2004
Multiple recent horizontal transfers of a large genomic region in cheese making fungi Cheeseman, Kevin; Ropars, Jeanne; Renault, Pierre Nature Communications, Vol. 5, Issue 1 https://doi.org/10.1038/ncomms3876	journal	January 2014
High throughput ANI analysis of 90K prokaryotic genomes reveals clear species boundaries Jain, Chirag; Rodriguez-R, Luis M.; Phillippy, Adam M. Nature Communications, Vol. 9, Issue 1 https://doi.org/10.1038/s41467-018-07641-9	journal	November 2018
Fungal secondary metabolism: regulation, function and drug discovery Keller, Nancy P. Nature Reviews Microbiology, Vol. 17, Issue 3 https://doi.org/10.1038/s41579-018-0121-1	journal	December 2018
Assembly of long, error-prone reads using repeat graphs Kolmogorov, Mikhail; Yuan, Jeffrey; Lin, Yu Nature Biotechnology, Vol. 37, Issue 5 https://doi.org/10.1038/s41587-019-0072-8	journal	April 2019
Accurate prediction of secondary metabolite gene clusters in filamentous fungi Andersen, M. R.; Nielsen, J. B.; Klitgaard, A. Proceedings of the National Academy of Sciences, Vol. 110, Issue 1 https://doi.org/10.1073/pnas.1205532110	journal	December 2012
RepeatModeler2 for automated genomic discovery of transposable element families Flynn, Jullien M.; Hubley, Robert; Goubert, Clément Proceedings of the National Academy of Sciences, Vol. 117, Issue 17 https://doi.org/10.1073/pnas.1921046117	journal	April 2020
Secondary metabolism in Penicillium expansum : Emphasis on recent advances in patulin research Tannous, Joanna; Keller, Nancy P.; Atoui, Ali Critical Reviews in Food Science and Nutrition, Vol. 58, Issue 12 https://doi.org/10.1080/10408398.2017.1305945	journal	June 2017
Infernal 1.1: 100-fold faster RNA homology searches Nawrocki, E. P.; Eddy, S. R. Bioinformatics, Vol. 29, Issue 22 https://doi.org/10.1093/bioinformatics/btt509	journal	September 2013
InterProScan 5: genome-scale protein function classification Jones, P.; Binns, D.; Chang, H. -Y. Bioinformatics, Vol. 30, Issue 9 https://doi.org/10.1093/bioinformatics/btu031	journal	January 2014
BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs Simão, Felipe A.; Waterhouse, Robert M.; Ioannidis, Panagiotis Bioinformatics, Vol. 31, Issue 19 https://doi.org/10.1093/bioinformatics/btv351	journal	June 2015
NanoPack: visualizing and processing long-read sequencing data De Coster, Wouter; D’Hert, Svenn; Schultz, Darrin T. Bioinformatics, Vol. 34, Issue 15 https://doi.org/10.1093/bioinformatics/bty149	journal	March 2018
Management of postharvest blue mould of apple caused by Penicillium fuscoglaucum using a gel formulation containing Monarda citriodora essential oil and linalool Rani, Pragya; Sharma, Mohini; Poovathumkadavil Thambi, Nidhin Journal of Applied Microbiology, Vol. 134, Issue 4 https://doi.org/10.1093/jambio/lxad068	journal	April 2023
antiSMASH 6.0: improving cluster detection and comparison capabilities Blin, Kai; Shaw, Simon; Kloosterman, Alexander M. Nucleic Acids Research, Vol. 49, Issue W1 https://doi.org/10.1093/nar/gkab335	journal	May 2021
Improved Genome Assembly Resource of the Plant Pathogen Fusarium avenaceum Gottschalk, Christopher; Evans, Breyn; Collum, Tamara D. PhytoFrontiers™, Vol. 3, Issue 2 https://doi.org/10.1094/PHYTOFR-10-22-0117-A	journal	September 2023
Impact ofveAon the development, aggressiveness, dissemination and secondary metabolism ofPenicillium expansum El Hajj Assaf, Christelle; Snini, Selma P.; Tadrist, Souria Molecular Plant Pathology, Vol. 19, Issue 8 https://doi.org/10.1111/mpp.12673	journal	April 2018
Penicillium expansum: biology, omics, and management tools for a global postharvest pathogen causing blue mould of pome fruit Luciano‐Rosario, Dianiris; Keller, Nancy P.; Jurick, Wayne M. Molecular Plant Pathology, Vol. 21, Issue 11 https://doi.org/10.1111/mpp.12990	journal	September 2020
A Robust Phylogenomic Time Tree for Biotechnologically and Medically Important Fungi in the Genera Aspergillus and Penicillium Steenwyk, Jacob L.; Shen, Xing-Xing; Lind, Abigail L. mBio, Vol. 10, Issue 4 https://doi.org/10.1128/mBio.00925-19	journal	August 2019
BLAST+: architecture and applications Camacho, Christiam; Coulouris, George; Avagyan, Vahram BMC Bioinformatics, Vol. 10, Issue 1 https://doi.org/10.1186/1471-2105-10-421	journal	January 2009
MAKER2: an annotation pipeline and genome-database management tool for second-generation genome projects Holt, Carson; Yandell, Mark BMC Bioinformatics, Vol. 12, Issue 1 https://doi.org/10.1186/1471-2105-12-491	journal	December 2011
Comparative genomic study of the Penicillium genus elucidates a diverse pangenome and 15 lateral gene transfer events Petersen, Celine; Sørensen, Trine; Nielsen, Mikkel R. IMA Fungus, Vol. 14, Issue 1 https://doi.org/10.1186/s43008-023-00108-7	journal	February 2023
IMA genome-F18 Visagie, Cobus M.; Magistà, Donato; Ferrara, Massimo IMA Fungus, Vol. 14, Issue 1 https://doi.org/10.1186/s43008-023-00121-w	journal	October 2023
New Insight Into Pathogenicity and Secondary Metabolism of the Plant Pathogen Penicillium expansum Through Deletion of the Epigenetic Reader SntB Tannous, Joanna; Barda, Omer; Luciano-Rosario, Dianiris Frontiers in Microbiology, Vol. 11 https://doi.org/10.3389/fmicb.2020.00610	journal	April 2020
PR Toxin – Biosynthesis, Genetic Regulation, Toxicological Potential, Prevention and Control Measures: Overview and Challenges Dubey, Manish K.; Aamir, Mohd; Kaushik, Manish S. Frontiers in Pharmacology, Vol. 9 https://doi.org/10.3389/fphar.2018.00288	journal	March 2018
Insight into the Genome of Diverse Penicillium chrysogenum Strains: Specific Genes, Cluster Duplications and DNA Fragment Translocations Martín, Juan F. International Journal of Molecular Sciences, Vol. 21, Issue 11 https://doi.org/10.3390/ijms21113936	journal	May 2020
Mining the Penicillium expansum Genome for Virulence Genes: A Functional-Based Approach to Discover Novel Loci Mediating Blue Mold Decay of Apple Fruit Luciano-Rosario, Dianiris; Peng, Hui; Gaskins, Verneta L. Journal of Fungi, Vol. 9, Issue 11 https://doi.org/10.3390/jof9111066	journal	November 2023
Avirulent Isolates of Penicillium chrysogenum to Control the Blue Mold of Apple Caused by P. expansum Bartholomew, Holly P.; Luciano-Rosario, Dianiris; Bradshaw, Michael J. Microorganisms, Vol. 11, Issue 11 https://doi.org/10.3390/microorganisms11112792	journal	November 2023
Cyclopiazonic Acid Biosynthesis of Aspergillus flavus and Aspergillus oryzae Chang, Perng-Kuang; Ehrlich, Kenneth; Fujii, Isao Toxins, Vol. 1, Issue 2 https://doi.org/10.3390/toxins1020074	journal	November 2009
Production of Cyclopiazonic Acid by Penicillium commune Isolated from Dry-Cured Ham on a Meat Extract–Based Substrate Sosa, María J.; Córdoba, Juan J.; Díaz, Carmen Journal of Food Protection, Vol. 65, Issue 6 https://doi.org/10.4315/0362-028X-65.6.988	journal	June 2002
D-GENIES: dot plot large genomes in an interactive, efficient and simple way Cabanettes, Floréal; Klopp, Christophe PeerJ, Vol. 6 https://doi.org/10.7717/peerj.4958	journal	January 2018
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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Title: The Near-Gapless Penicillium fuscoglaucum Genome Enables the Discovery of Lifestyle Features as an Emerging Post-Harvest Phytopathogen

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