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.; Gaskins, Verneta L.; Peng, Hui; Fonseca, Jorge M.; Jurick II, Wayne M.

doi:10.3390/microorganisms11112792

Avirulent Isolates of Penicillium chrysogenum to Control the Blue Mold of Apple Caused by P. expansum

Journal Article · Fri Nov 17 00:00:00 EST 2023 · Microorganisms

DOI:https://doi.org/10.3390/microorganisms11112792· OSTI ID:2471236

^[1]; Luciano-Rosario, Dianiris ^[1]; ^[2]; Gaskins, Verneta L. ^[1]; Peng, Hui ^[1]; ^[1]; Jurick II, Wayne M. ^[1]

US Dept. of Agriculture (USDA), Beltsville, MD (United States). Agricultural Research Service (ARS), Beltsville Agricultural Research Center
Harvard University, Cambridge, MA (United States)

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 chrysogenum isolates, 404 and 413, were investigated as potential biocontrol agents against P. expansum in apple. Notably, 404 and 413 were non-pathogenic in apple, yet they grew vigorously 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 the subsequent co-inoculation of R19 or Pe21 simultaneously, 3, or 7 days after prior inoculation with 404 or 413. The co-inoculation of these isolates showed reduced decay incidence and severity, with the most significant reduction from the longer establishment of P. chrysogenum. In vitro growth showed no antagonism between species, further suggesting competitive niche colonization as the mode of action for decay reduction. Both P. chrysogenum isolates had incomplete patulin gene clusters but tolerated patulin treatment. Finally, hygromycin resistance was observed for both P. chrysogenum isolates, yet they are not multiresistant 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.

View Accepted Manuscript (DOE)

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

Sponsoring Organization:: USDOE Office of Science (SC)

Grant/Contract Number:: SC0014664

OSTI ID:: 2471236

Journal Information:: Microorganisms, Journal Name: Microorganisms Journal Issue: 11 Vol. 11; ISSN 2076-2607

Publisher:: MDPICopyright Statement

Country of Publication:: United States

Language:: English

References (62)

Production of patulin by Micromycetes Steiman, R.; Seigle-Murandi, F.; Sage, L. Mycopathologia, Vol. 105, Issue 3 https://doi.org/10.1007/BF00437244	journal	March 1989
Development and commercial use of afla-Guard®, an aflatoxin biocontrol agent Dorner, J. W.; Lamb, M. C. Mycotoxin Research, Vol. 22, Issue 1 https://doi.org/10.1007/BF02954555	journal	March 2006
An assessment of the air quality in apple warehouses: new records of Aspergillus europaeus, Aspergillus pulverulentus, Penicillium allii and Penicillium sumatraense as decay agents Smiri, Marwa; Kheireddine, Amina; Hammami, Rania Archives of Microbiology, Vol. 203, Issue 10 https://doi.org/10.1007/s00203-021-02551-9	journal	September 2021
Biological control of postharvest diseases by microbial antagonists: how many mechanisms of action? Di Francesco, A.; Martini, C.; Mari, M. European Journal of Plant Pathology, Vol. 145, Issue 4 https://doi.org/10.1007/s10658-016-0867-0	journal	January 2016
raxmlGUI: a graphical front-end for RAxML Silvestro, Daniele; Michalak, Ingo Organisms Diversity & Evolution, Vol. 12, Issue 4 https://doi.org/10.1007/s13127-011-0056-0	journal	September 2011
[39] Transformation of filamentous fungi based on hygromycin b and phleomycin resistance markers Punt, Peter J.; van den Hondel, Cees A. M. J. J. Methods in Enzymology https://doi.org/10.1016/0076-6879(92)16041-H	book	January 1992
Plasmid-encoded hygromycin B resistance: the sequence of hygromycin B phosphotransferase gene and its expression in Escherichia coli and Saccharomyces cerevisiae Gritz, Linda; Davies, Julian Gene, Vol. 25, Issue 2-3 https://doi.org/10.1016/0378-1119(83)90223-8	journal	November 1983
Evaluation of genotoxic risk and oxidative DNA damage in mammalian cells exposed to mycotoxins, patulin and citrinin Liu, Biing-Hui; Yu, Feng-Yih; Wu, Ting-Shuan Toxicology and Applied Pharmacology, Vol. 191, Issue 3 https://doi.org/10.1016/S0041-008X(03)00254-0	journal	September 2003
Biological and integrated control of postharvest blue mold (Penicillium expansum) of apples by Pseudomonas syringae and cyprodinil Errampalli, Deena; Brubacher, Nichole R. Biological Control, Vol. 36, Issue 1 https://doi.org/10.1016/j.biocontrol.2005.07.011	journal	January 2006
Regulation of multidrug resistance in pathogenic fungi Morschhäuser, Joachim Fungal Genetics and Biology, Vol. 47, Issue 2 https://doi.org/10.1016/j.fgb.2009.08.002	journal	February 2010
Evaluation of the activity of the antifungal PgAFP protein and its producer mould against Penicillium spp postharvest pathogens of citrus and pome fruits Delgado, Josué; Ballester, Ana-Rosa; Núñez, Félix Food Microbiology, Vol. 84 https://doi.org/10.1016/j.fm.2019.103266	journal	December 2019
Occurrence of toxin-producing fungi in intact and rotten table and wine grapes and related influencing factors Chunmei, Jiang; Junling, Shi; Qi'an, Han Food Control, Vol. 31, Issue 1 https://doi.org/10.1016/j.foodcont.2012.09.015	journal	May 2013
Sequencing, physical organization and kinetic expression of the patulin biosynthetic gene cluster from Penicillium expansum Tannous, Joanna; El Khoury, Rhoda; Snini, Selma P. International Journal of Food Microbiology, Vol. 189 https://doi.org/10.1016/j.ijfoodmicro.2014.07.028	journal	October 2014
Growth inhibition and stability of PgAFP from Penicillium chrysogenum against fungi common on dry-ripened meat products Delgado, Josué; Acosta, Raquel; Rodríguez-Martín, Andrea International Journal of Food Microbiology, Vol. 205 https://doi.org/10.1016/j.ijfoodmicro.2015.03.029	journal	July 2015
Molecular characterization of patulin producing and non-producing Penicillium species in apples from Morocco Rharmitt, Sanae; Hafidi, Majida; Hajjaj, Hassan International Journal of Food Microbiology, Vol. 217 https://doi.org/10.1016/j.ijfoodmicro.2015.10.019	journal	January 2016
Biocontrol of Penicillium griseofulvum to reduce cyclopiazonic acid contamination in dry-fermented sausages Delgado, Josué; Peromingo, Belén; Rodríguez, Alicia International Journal of Food Microbiology, Vol. 293 https://doi.org/10.1016/j.ijfoodmicro.2018.12.027	journal	March 2019
Multidrug resistance of Penicillium expansum to fungicides: whole transcriptome analysis of MDR strains reveals overexpression of efflux transporter genes Samaras, Αnastasios; Ntasiou, Panagiota; Myresiotis, Charalampos International Journal of Food Microbiology, Vol. 335 https://doi.org/10.1016/j.ijfoodmicro.2020.108896	journal	December 2020
Study on the biocontrol effect and physiological mechanism of Hannaella sinensis on the blue mold decay of apples Lin, Rouling; Yang, Qiya; Xiao, Jinwei International Journal of Food Microbiology, Vol. 382 https://doi.org/10.1016/j.ijfoodmicro.2022.109931	journal	December 2022
The conditioned reconstructed process Gernhard, Tanja Journal of Theoretical Biology, Vol. 253, Issue 4 https://doi.org/10.1016/j.jtbi.2008.04.005	journal	August 2008
Characterization of boscalid-resistance conferring mutations in the Sdh B subunit of respiratory complex II and impact on fitness and mycotoxin production in Penicillium expansum laboratory strains Malandrakis, Anastasios A.; Vattis, Konstantinos N.; Markoglou, Anastasios N. Pesticide Biochemistry and Physiology, Vol. 138 https://doi.org/10.1016/j.pestbp.2017.03.009	journal	May 2017
Baseline sensitivities to fludioxonil and pyrimethanil in Penicillium expansum populations from apple in Washington State Li, H. X.; Xiao, C. L. Postharvest Biology and Technology, Vol. 47, Issue 2 https://doi.org/10.1016/j.postharvbio.2007.06.022	journal	February 2008
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
Molecular identification of isolated fungi from stored apples in Riyadh, Saudi Arabia Alwakeel, Suaad S. Saudi Journal of Biological Sciences, Vol. 20, Issue 4 https://doi.org/10.1016/j.sjbs.2013.05.002	journal	October 2013
Patulin-induced oxidative DNA damage and p53 modulation in HepG2 cells Zhou, Si-min; Jiang, Li-ping; Geng, Cheng-yan Toxicon, Vol. 55, Issue 2-3 https://doi.org/10.1016/j.toxicon.2009.08.019	journal	February 2010
Model selection may not be a mandatory step for phylogeny reconstruction Abadi, Shiran; Azouri, Dana; Pupko, Tal Nature Communications, Vol. 10, Issue 1 https://doi.org/10.1038/s41467-019-08822-w	journal	February 2019
Toxicological effects of patulin mycotoxin on the mammalian system: an overview Pal, Saurabh; Singh, Neha; Ansari, Kausar Mahmood Toxicology Research, Vol. 6, Issue 6 https://doi.org/10.1039/c7tx00138j	journal	September 2017
Structure and Function of APH(4)-Ia, a Hygromycin B Resistance Enzyme Stogios, Peter J.; Shakya, Tushar; Evdokimova, Elena Journal of Biological Chemistry, Vol. 286, Issue 3 https://doi.org/10.1074/jbc.M110.194266	journal	January 2011
Blistering1 Modulates Penicillium expansum Virulence Via Vesicle-mediated Protein Secretion Jurick, Wayne M.; Peng, Hui; Beard, Hunter S. Molecular & Cellular Proteomics, Vol. 19, Issue 2 https://doi.org/10.1074/mcp.RA119.001831	journal	February 2020
MEGA11: Molecular Evolutionary Genetics Analysis Version 11 Tamura, Koichiro; Stecher, Glen; Kumar, Sudhir Molecular Biology and Evolution, Vol. 38, Issue 7 https://doi.org/10.1093/molbev/msab120	journal	April 2021
Bayesian phylogenetic and phylodynamic data integration using BEAST 1.10 Suchard, Marc A.; Lemey, Philippe; Baele, Guy Virus Evolution, Vol. 4, Issue 1 https://doi.org/10.1093/ve/vey016	journal	January 2018
Genome, Transcriptome, and Functional Analyses of Penicillium expansum Provide New Insights Into Secondary Metabolism and Pathogenicity Ballester, Ana-Rosa; Marcet-Houben, Marina; Levin, Elena Molecular Plant-Microbe Interactions®, Vol. 28, Issue 3 https://doi.org/10.1094/MPMI-09-14-0261-FI	journal	March 2015
Baseline Sensitivity of Penicillium spp. to Difenoconazole Jurick, Wayne M.; Macarisin, Otilia; Gaskins, Verneta L. Plant Disease, Vol. 103, Issue 2 https://doi.org/10.1094/PDIS-05-18-0860-RE	journal	February 2019
Pathogenic Penicillium spp. on Apple and Pear Louw, Johannes Petrus; Korsten, Lise Plant Disease, Vol. 98, Issue 5 https://doi.org/10.1094/PDIS-07-13-0710-RE	journal	May 2014
First Report of Penicillium expansum Isolates With Reduced Sensitivity to Fludioxonil From a Commercial Packinghouse in Pennsylvania Gaskins, V. L.; Vico, I.; Yu, J. Plant Disease, Vol. 99, Issue 8 https://doi.org/10.1094/PDIS-11-14-1161-PDN	journal	August 2015
First Report of Penicillium expansum Isolates Resistant to Pyrimethanil from Stored Apple Fruit in Pennsylvania Yan, H. J.; Gaskins, V. L.; Vico, I. Plant Disease, Vol. 98, Issue 7 https://doi.org/10.1094/PDIS-12-13-1214-PDN	journal	July 2014
More than a Virulence Factor: Patulin Is a Non-Host-Specific Toxin that Inhibits Postharvest Phytopathogens and Requires Efflux for Penicillium Tolerance Bartholomew, Holly P.; Bradshaw, Michael J.; Macarisin, Otilia Phytopathology®, Vol. 112, Issue 5 https://doi.org/10.1094/PHYTO-09-21-0371-R	journal	May 2022
Penicillium digitatumSuppresses Production of Hydrogen Peroxide in Host Tissue During Infection of Citrus Fruit Macarisin, D.; Cohen, L.; Eick, A. Phytopathology®, Vol. 97, Issue 11 https://doi.org/10.1094/PHYTO-97-11-1491	journal	November 2007
Involvement of Gluconic Acid and Glucose Oxidase in the Pathogenicity of Penicillium expansum in Apples Hadas, Yoav; Goldberg, Israel; Pines, Ophry Phytopathology®, Vol. 97, Issue 3 https://doi.org/10.1094/PHYTO-97-3-0384	journal	March 2007
Development of Spontaneous Hygromycin B Resistance in Monilinia fructicola and Its Impact on Growth Rate, Morphology, Susceptibility to Demethylation Inhibitor Fungicides, and Sporulation Dai, Qun; Sun, Zhihuan; Schnabel, Guido Phytopathology®, Vol. 93, Issue 11 https://doi.org/10.1094/PHYTO.2003.93.11.1354	journal	November 2003
Structural basis for the substrate recognition of aminoglycoside 7′′-phosphotransferase-Ia from Streptomyces hygroscopicus Takenoya, Mihoko; Shimamura, Tatsuro; Yamanaka, Ryuji Acta Crystallographica Section F Structural Biology Communications, Vol. 75, Issue 9 https://doi.org/10.1107/S2053230X19011105	journal	August 2019
Diversity and population dynamics of Penicillium spp. on apples in pre‐ and postharvest environments: consequences for decay development Amiri, A.; Bompeix, G. Plant Pathology, Vol. 54, Issue 1 https://doi.org/10.1111/j.1365-3059.2005.01112.x	journal	January 2005
New Names for Three Penicillium Strains Based on Updated Barcoding and Phylogenetic Analyses Yin, Guohua; Jurick, Wayne M.; Zhao, Guozhu Microbiology Resource Announcements, Vol. 10, Issue 48 https://doi.org/10.1128/MRA.00466-21	journal	December 2021
Draft Genome Sequence of Penicillium expansum Strain R19, Which Causes Postharvest Decay of Apple Fruit Yu, Jiujiang; Jurick, Wayne M.; Cao, Huansheng Genome Announcements, Vol. 2, Issue 3 https://doi.org/10.1128/genomeA.00635-14	journal	June 2014
Global transcriptomic responses orchestrate difenoconazole resistance in Penicillium spp. causing blue mold of stored apple fruit Lichtner, Franz J.; Gaskins, Verneta L.; Cox, Kerik D. BMC Genomics, Vol. 21, Issue 1 https://doi.org/10.1186/s12864-020-06987-z	journal	August 2020
Blocking drug efflux mechanisms facilitate genome engineering process in hypercellulolytic fungus, Penicillium funiculosum NCIM1228 Randhawa, Anmoldeep; Pasari, Nandita; Sinha, Tulika Biotechnology for Biofuels, Vol. 14, Issue 1 https://doi.org/10.1186/s13068-021-01883-4	journal	January 2021
Efflux in Fungi: La Pièce de Résistance Coleman, Jeffrey J.; Mylonakis, Eleftherios PLoS Pathogens, Vol. 5, Issue 6 https://doi.org/10.1371/journal.ppat.1000486	journal	June 2009
Confidence Limits on Phylogenies: An Approach Using the Bootstrap Felsenstein, Joseph Evolution, Vol. 39, Issue 4, p. 783-791 https://doi.org/10.2307/2408678	journal	July 1985
Selection Pressure Pathways and Mechanisms of Resistance to the Demethylation Inhibitor-Difenoconazole in Penicillium expansum Ali, Emran Md; Amiri, Achour Frontiers in Microbiology, Vol. 9 https://doi.org/10.3389/fmicb.2018.02472	journal	October 2018
Modes of Action of Microbial Biocontrol in the Phyllosphere Legein, Marie; Smets, Wenke; Vandenheuvel, Dieter Frontiers in Microbiology, Vol. 11 https://doi.org/10.3389/fmicb.2020.01619	journal	July 2020
The Good, the Bad, and the Ugly: Mycotoxin Production During Postharvest Decay and Their Influence on Tritrophic Host–Pathogen–Microbe Interactions Bartholomew, Holly P.; Bradshaw, Michael; Jurick, Wayne M. Frontiers in Microbiology, Vol. 12 https://doi.org/10.3389/fmicb.2021.611881	journal	February 2021
Reducing Postharvest Losses during Storage of Grain Crops to Strengthen Food Security in Developing Countries Kumar, Deepak; Kalita, Prasanta Foods, Vol. 6, Issue 1 https://doi.org/10.3390/foods6010008	journal	January 2017
Effects of Preservative Agents on Quality Attributes of Dry-Cured Fermented Sausages Álvarez, Micaela; Andrade, María J.; García, Carmen Foods, Vol. 9, Issue 10 https://doi.org/10.3390/foods9101505	journal	October 2020
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
Genomic Analyses of Penicillium Species Have Revealed Patulin and Citrinin Gene Clusters and Novel Loci Involved in Oxylipin Production Yin, Guohua; Zhao, Hui; Pennerman, Kayla K. Journal of Fungi, Vol. 7, Issue 9 https://doi.org/10.3390/jof7090743	journal	September 2021
Comparative Penicillium spp. Transcriptomics: Conserved Pathways and Processes Revealed in Ungerminated Conidia and during Postharvest Apple Fruit Decay Bartholomew, Holly P.; Lichtner, Franz J.; Bradshaw, Michael Microorganisms, Vol. 10, Issue 12 https://doi.org/10.3390/microorganisms10122414	journal	December 2022
Non-Target Site Mechanisms of Fungicide Resistance in Crop Pathogens: A Review Hu, Mengjun; Chen, Shuning Microorganisms, Vol. 9, Issue 3 https://doi.org/10.3390/microorganisms9030502	journal	February 2021
Efficacy of the Combined Protective Cultures of Penicillium chrysogenum and Debaryomyces hansenii for the Control of Ochratoxin A Hazard in Dry-Cured Ham Cebrián, Eva; Rodríguez, Mar; Peromingo, Belén Toxins, Vol. 11, Issue 12 https://doi.org/10.3390/toxins11120710	journal	December 2019
Biosynthesis and Toxicological Effects of Patulin Puel, Olivier; Galtier, Pierre; Oswald, Isabelle Toxins, Vol. 2, Issue 4 https://doi.org/10.3390/toxins2040613	journal	April 2010
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
New penicillin-producing Penicillium species and an overview of section Chrysogena Houbraken, J.; Frisvad, J. C.; Seifert, K. A. Persoonia - Molecular Phylogeny and Evolution of Fungi, Vol. 29, Issue 1 https://doi.org/10.3767/003158512X660571	journal	December 2012
Fleming’s penicillin producing strain is not Penicillium chrysogenum but P. rubens Houbraken, Jos; Frisvad, Jens C.; Samson, Robert A. IMA Fungus, Vol. 2, Issue 1 https://doi.org/10.5598/imafungus.2011.02.01.12	journal	June 2011
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

Similar Records

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

Journal Article · Fri Dec 27 19:00:00 EST 2024 · Journal of Fungi · OSTI ID:2484207

Patulin Inhibition of Specific Apple Microbiome Members Uncovers Hanseniaspora uvarum as a Potential Biocontrol Agent

Journal Article · Fri Jan 31 19:00:00 EST 2025 · Phytopathology® · OSTI ID:3014195

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
Microbiology
Penicillium chrysogenum
Penicillium expansum
apple fruit
biocontrol
blue mold
mycotoxin
patulin
postharvest decay

Avirulent Isolates of Penicillium chrysogenum to Control the Blue Mold of Apple Caused by P. expansum

Citation Formats

References (62)

Similar Records

Related Subjects