Microevolution in the pansecondary metabolome of Aspergillus flavus and its potential macroevolutionary implications for filamentous fungi

Drott, Milton T.; Rush, Tomás A.; Satterlee, Tatum R.; Giannone, Richard J.; Abraham, Paul E.; Greco, Claudio; Venkatesh, Nandhitha; Skerker, Jeffrey M.; Glass, N. Louise; Labbé, Jesse L.; Milgroom, Michael G.; Keller, Nancy P.

doi:10.1073/pnas.2021683118

Title: Microevolution in the pansecondary metabolome of Aspergillus flavus and its potential macroevolutionary implications for filamentous fungi

Journal Article · Thu May 20 00:00:00 EDT 2021 · Proceedings of the National Academy of Sciences of the United States of America

DOI:https://doi.org/10.1073/pnas.2021683118· OSTI ID:1847996

^[1];

^[2]; Satterlee, Tatum R. ^[3];

^[2]; Abraham, Paul E. ^[2];

^[4]; Venkatesh, Nandhitha ^[5]; Skerker, Jeffrey M. ^[6];

^[7];

^[2];

^[8];

^[9]

Department of Bacteriology, University of Wisconsin–Madison, Madison, WI 53703,
Biosciences Division, Oak Ridge National Laboratory, Oak Ridge, TN 37830,
Department of Genetics, University of Wisconsin–Madison, Madison, WI 53703,
Department of Molecular Microbiology, John Innes Centre, Norwich, NR4 7UH, United Kingdom,
Department of Medical Microbiology and Immunology, University of Wisconsin–Madison, Madison, WI 53703,, Department of Plant Pathology, University of Wisconsin–Madison, Madison, WI 53706,
Innovative Genomics Institute, University of California, Berkeley, CA 94720,
Innovative Genomics Institute, University of California, Berkeley, CA 94720,, Department of Plant and Microbial Biology, University of California, Berkeley, CA 94720,, Environmental Genomics and Systems Biology, The Lawrence Berkeley National Laboratory, Berkeley, CA 94720,
School of Integrative Plant Science, Cornell University, Ithaca, NY 14853
Department of Bacteriology, University of Wisconsin–Madison, Madison, WI 53703,, Department of Medical Microbiology and Immunology, University of Wisconsin–Madison, Madison, WI 53703,

Fungi produce a wealth of pharmacologically bioactive secondary metabolites (SMs) from biosynthetic gene clusters (BGCs). It is common practice for drug discovery efforts to treat species’ secondary metabolomes as being well represented by a single or a small number of representative genomes. However, this approach misses the possibility that intraspecific population dynamics, such as adaptation to environmental conditions or local microbiomes, may harbor novel BGCs that contribute to the overall niche breadth of species. Using 94 isolates of Aspergillus flavus, a cosmopolitan model fungus, sampled from seven states in the United States, we dereplicate 7,821 BGCs into 92 unique BGCs. We find that more than 25% of pangenomic BGCs show population-specific patterns of presence/absence or protein divergence. Population-specific BGCs make up most of the accessory-genome BGCs, suggesting that different ecological forces that maintain accessory genomes may be partially mediated by population-specific differences in secondary metabolism. We use ultra-high-performance high-resolution mass spectrometry to confirm that these genetic differences in BGCs also result in chemotypic differences in SM production in different populations, which could mediate ecological interactions and be acted on by selection. Thus, our results suggest a paradigm shift that previously unrealized population-level reservoirs of SM diversity may be of significant evolutionary, ecological, and pharmacological importance. Finally, we find that several population-specific BGCs from A. flavus are present in Aspergillus parasiticus and Aspergillus minisclerotigenes and discuss how the microevolutionary patterns we uncover inform macroevolutionary inferences and help to align fungal secondary metabolism with existing evolutionary theory.

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Research Organization:: Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER); USDA

Grant/Contract Number:: AC05-00OR22725; 2019-67012-29662

OSTI ID:: 1847996

Alternate ID(s):: OSTI ID: 1785198

Journal Information:: Proceedings of the National Academy of Sciences of the United States of America, Journal Name: Proceedings of the National Academy of Sciences of the United States of America Vol. 118 Journal Issue: 21; ISSN 0027-8424

Publisher:: Proceedings of the National Academy of SciencesCopyright Statement

Country of Publication:: United States

Language:: English

References (75)

Population structure promotes the evolution of costly sex in artificial gene networks Whitlock, Alexander O. B.; Azevedo, Ricardo B. R.; Burch, Christina L. Evolution, Vol. 73, Issue 6 https://doi.org/10.1111/evo.13733	journal	April 2019
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
Population Genetics of Fusarium graminearum at the Interface of Wheat and Wild Grass Communities in New York Fulcher, Michael R.; Winans, James B.; Quan, Menchus Phytopathology®, Vol. 109, Issue 12 https://doi.org/10.1094/PHYTO-05-19-0169-R	journal	December 2019
Characterization of the biosynthetic gene cluster for the ribosomally synthesized cyclic peptide ustiloxin B in Aspergillus flavus Umemura, Myco; Nagano, Nozomi; Koike, Hideaki Fungal Genetics and Biology, Vol. 68 https://doi.org/10.1016/j.fgb.2014.04.011	journal	July 2014
Clues to an Evolutionary Mystery: The Genes for T-Toxin, Enabler of the Devastating 1970 Southern Corn Leaf Blight Epidemic, Are Present in Ancestral Species, Suggesting an Ancient Origin Condon, Bradford J.; Elliott, Candace; González, Jonathan B. Molecular Plant-Microbe Interactions®, Vol. 31, Issue 11 https://doi.org/10.1094/MPMI-03-18-0070-R	journal	November 2018
Investigation of inter- and intraspecies variation through genome sequencing of Aspergillus section Nigri Vesth, Tammi C.; Nybo, Jane L.; Theobald, Sebastian Nature Genetics, Vol. 50, Issue 12 https://doi.org/10.1038/s41588-018-0246-1	journal	October 2018
Ancestral polymorphism and adaptive evolution in the trichothecene mycotoxin gene cluster of phytopathogenic Fusarium Ward, T. J.; Bielawski, J. P.; Kistler, H. C. Proceedings of the National Academy of Sciences, Vol. 99, Issue 14 https://doi.org/10.1073/pnas.142307199	journal	June 2002
Comparative genomics and transcriptomics depict ericoid mycorrhizal fungi as versatile saprotrophs and plant mutualists Martino, Elena; Morin, Emmanuelle; Grelet, Gwen-Aëlle New Phytologist, Vol. 217, Issue 3 https://doi.org/10.1111/nph.14974	journal	January 2018
Population structure, genetic diversity, and sexual state of the rice brown spot pathogen Bipolaris oryzae from three Asian countries Ahmadpour, A.; Castell-Miller, C.; Javan-Nikkhah, M. Plant Pathology, Vol. 67, Issue 1 https://doi.org/10.1111/ppa.12714	journal	May 2017
The Population Genetics of dN/dS Kryazhimskiy, Sergey; Plotkin, Joshua B. PLoS Genetics, Vol. 4, Issue 12 https://doi.org/10.1371/journal.pgen.1000304	journal	December 2008
Biodiversity of *Aspergillus* section *Flavi* in the United States: A review Horn, Bruce W. Food Additives and Contaminants, Vol. 24, Issue 10 https://doi.org/10.1080/02652030701510012	journal	October 2007
Cytochrome P450 as Dimerization Catalyst in Diketopiperazine Alkaloid Biosynthesis Saruwatari, Takayoshi; Yagishita, Fumitoshi; Mino, Takashi ChemBioChem, Vol. 15, Issue 5 https://doi.org/10.1002/cbic.201300751	journal	February 2014
Mycotoxins and human disease: a largely ignored global health issue Wild, C. P.; Gong, Y. Y. Carcinogenesis, Vol. 31, Issue 1 https://doi.org/10.1093/carcin/bgp264	journal	October 2009
Homologous NRPS-like Gene Clusters Mediate Redundant Small-Molecule Biosynthesis in Aspergillus flavus Forseth, Ry R.; Amaike, Saori; Schwenk, Daniel Angewandte Chemie International Edition, Vol. 52, Issue 5 https://doi.org/10.1002/anie.201207456	journal	December 2012
ggplot2 Wickham, Hadley Use R! https://doi.org/10.1007/978-3-319-24277-4	book	January 2016
Secondary Metabolism and Biotrophic Lifestyle in the Tomato Pathogen Cladosporium fulvum Collemare, Jérôme; Griffiths, Scott; Iida, Yuichiro PLoS ONE, Vol. 9, Issue 1 https://doi.org/10.1371/journal.pone.0085877	journal	January 2014
MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) Software Version 4.0 Tamura, K.; Dudley, J.; Nei, M. Molecular Biology and Evolution, Vol. 24, Issue 8 https://doi.org/10.1093/molbev/msm092	journal	April 2007
Functional characterization of a veA-dependent polyketide synthase gene in Aspergillus flavus necessary for the synthesis of asparasone, a sclerotium-specific pigment Cary, Jeffrey W.; Harris-Coward, Pamela Y.; Ehrlich, Kenneth C. Fungal Genetics and Biology, Vol. 64 https://doi.org/10.1016/j.fgb.2014.01.001	journal	March 2014
Population Subdivision and the Frequency of Aflatoxigenic Isolates in Aspergillus flavus in the United States Drott, Milton T.; Fessler, Lauren M.; Milgroom, Michael G. Phytopathology®, Vol. 109, Issue 5 https://doi.org/10.1094/PHYTO-07-18-0263-R	journal	May 2019
Comparative Genomics of Aspergillus flavus S and L Morphotypes Yield Insights into Niche Adaptation Ohkura, Mana; Cotty, Peter J.; Orbach, Marc J. G3 Genes\|Genomes\|Genetics, Vol. 8, Issue 12 https://doi.org/10.1534/g3.118.200553	journal	December 2018
Spatial Genetic Structure and Population Dynamics of Gummy Stem Blight Fungi Within and Among Watermelon Fields in the Southeastern United States Li, Hao-Xi; Brewer, Marin Talbot Phytopathology®, Vol. 106, Issue 8 https://doi.org/10.1094/PHYTO-01-16-0006-R	journal	August 2016
Diversity of Secondary Metabolism in Aspergillus nidulans Clinical Isolates Drott, M. T.; Bastos, R. W.; Rokas, A. mSphere, Vol. 5, Issue 2 https://doi.org/10.1128/mSphere.00156-20	journal	April 2020
Copy number variation contributes to cryptic genetic variation in outbreak lineages of Cryptococcus gattii from the North American Pacific Northwest Steenwyk, Jacob L.; Soghigian, John S.; Perfect, John R. BMC Genomics, Vol. 17, Issue 1 https://doi.org/10.1186/s12864-016-3044-0	journal	September 2016
On the Emergence of Candida auris : Climate Change, Azoles, Swamps, and Birds Casadevall, Arturo; Kontoyiannis, Dimitrios P.; Robert, Vincent mBio, Vol. 10, Issue 4 https://doi.org/10.1128/mBio.01397-19	journal	July 2019
A comparative genomics study of 23 Aspergillus species from section Flavi Kjærbølling, Inge; Vesth, Tammi; Frisvad, Jens C. Nature Communications, Vol. 11, Issue 1 https://doi.org/10.1038/s41467-019-14051-y	journal	February 2020
The Ecology and Evolution of Pangenomes Brockhurst, Michael A.; Harrison, Ellie; Hall, James P. J. Current Biology, Vol. 29, Issue 20 https://doi.org/10.1016/j.cub.2019.08.012	journal	October 2019
Comparative Genomics of Bacillus amyloliquefaciens Strains Reveals a Core Genome with Traits for Habitat Adaptation and a Secondary Metabolites Rich Accessory Genome Belbahri, Lassaad; Chenari Bouket, Ali; Rekik, Imen Frontiers in Microbiology, Vol. 8 https://doi.org/10.3389/fmicb.2017.01438	journal	August 2017
Fitness Cost of Aflatoxin Production in Aspergillus flavus When Competing with Soil Microbes Could Maintain Balancing Selection Drott, Milton T.; Debenport, Tracy; Higgins, Steven A. mBio, Vol. 10, Issue 1 https://doi.org/10.1128/mBio.02782-18	journal	February 2019
Global Burden of Aflatoxin-Induced Hepatocellular Carcinoma: A Risk Assessment Liu, Yan; Wu, Felicia Environmental Health Perspectives, Vol. 118, Issue 6 https://doi.org/10.1289/ehp.0901388	journal	June 2010
The epigenetic reader SntB regulates secondary metabolism, development and global histone modifications in Aspergillus flavus Pfannenstiel, Brandon T.; Greco, Claudio; Sukowaty, Andrew T. Fungal Genetics and Biology, Vol. 120 https://doi.org/10.1016/j.fgb.2018.08.004	journal	November 2018
Trajectory and genomic determinants of fungal-pathogen speciation and host adaptation Hu, Xiao; Xiao, Guohua; Zheng, Peng Proceedings of the National Academy of Sciences, Vol. 111, Issue 47 https://doi.org/10.1073/pnas.1412662111	journal	November 2014
antiSMASH 4.0—improvements in chemistry prediction and gene cluster boundary identification Blin, Kai; Wolf, Thomas; Chevrette, Marc G. Nucleic Acids Research, Vol. 45, Issue W1 https://doi.org/10.1093/nar/gkx319	journal	April 2017
The geographic distribution and complex evolutionary history of the NX-2 trichothecene chemotype from Fusarium graminearum Kelly, Amy; Proctor, Robert H.; Belzile, Francois Fungal Genetics and Biology, Vol. 95 https://doi.org/10.1016/j.fgb.2016.08.003	journal	October 2016
Global Population Genetic Analysis of Aspergillus fumigatus Ashu, Eta Ebasi; Hagen, Ferry; Chowdhary, Anuradha mSphere, Vol. 2, Issue 1 https://doi.org/10.1128/mSphere.00019-17	journal	February 2017
NRPS-Derived Isoquinolines and Lipopetides Mediate Antagonism between Plant Pathogenic Fungi and Bacteria Khalid, Saima; Baccile, Joshua A.; Spraker, Joseph E. ACS Chemical Biology, Vol. 13, Issue 1 https://doi.org/10.1021/acschembio.7b00731	journal	December 2017
Linking secondary metabolites to gene clusters through genome sequencing of six diverse Aspergillus species Kjærbølling, Inge; Vesth, Tammi C.; Frisvad, Jens C. Proceedings of the National Academy of Sciences, Vol. 115, Issue 4 https://doi.org/10.1073/pnas.1715954115	journal	January 2018
Treeio: An R Package for Phylogenetic Tree Input and Output with Richly Annotated and Associated Data Wang, Li-Gen; Lam, Tommy Tsan-Yuk; Xu, Shuangbin Molecular Biology and Evolution, Vol. 37, Issue 2 https://doi.org/10.1093/molbev/msz240	journal	October 2019
Fusaristatin A production negatively affects the growth and aggressiveness of the wheat pathogen Fusarium pseudograminearum Khudhair, Mohammed; Kazan, Kemal; Thatcher, Louise F. Fungal Genetics and Biology, Vol. 136 https://doi.org/10.1016/j.fgb.2019.103314	journal	March 2020
Fungal secondary metabolism — from biochemistry to genomics Keller, Nancy P.; Turner, Geoffrey; Bennett, Joan W. Nature Reviews Microbiology, Vol. 3, Issue 12, p. 937-947 https://doi.org/10.1038/nrmicro1286	journal	December 2005
Clustered genes involved in cyclopiazonic acid production are next to the aflatoxin biosynthesis gene cluster in Aspergillus flavus Chang, Perng-Kuang; Horn, Bruce W.; Dorner, Joe W. Fungal Genetics and Biology, Vol. 46, Issue 2 https://doi.org/10.1016/j.fgb.2008.11.002	journal	February 2009
Drivers of genetic diversity in secondary metabolic gene clusters within a fungal species Lind, Abigail L.; Wisecaver, Jennifer H.; Lameiras, Catarina PLOS Biology, Vol. 15, Issue 11 https://doi.org/10.1371/journal.pbio.2003583	journal	November 2017
Genome sequencing and comparative genomics reveal a repertoire of putative pathogenicity genes in chilli anthracnose fungus Colletotrichum truncatum Rao, Soumya; Nandineni, Madhusudan R. PLOS ONE, Vol. 12, Issue 8 https://doi.org/10.1371/journal.pone.0183567	journal	August 2017
Identification of Two Aflatrem Biosynthesis Gene Loci in Aspergillus flavus and Metabolic Engineering of Penicillium paxilli To Elucidate Their Function Nicholson, M. J.; Koulman, A.; Monahan, B. J. Applied and Environmental Microbiology, Vol. 75, Issue 23 https://doi.org/10.1128/AEM.02146-08	journal	October 2009
Population genomics of Fusarium graminearum reveals signatures of divergent evolution within a major cereal pathogen Kelly, Amy C.; Ward, Todd J. PLOS ONE, Vol. 13, Issue 3 https://doi.org/10.1371/journal.pone.0194616	journal	March 2018
Depsipeptide Aspergillicins Revealed by Chromatin Reader Protein Deletion Greco, Claudio; Pfannenstiel, Brandon T.; Liu, James C. ACS Chemical Biology, Vol. 14, Issue 6 https://doi.org/10.1021/acschembio.9b00161	journal	May 2019
Cytoscape: A Software Environment for Integrated Models of Biomolecular Interaction Networks Shannon, P. Genome Research, Vol. 13, Issue 11 https://doi.org/10.1101/gr.1239303	journal	November 2003
Taxonomy of Aspergillus section Flavi and their production of aflatoxins, ochratoxins and other mycotoxins Frisvad, J. C.; Hubka, V.; Ezekiel, C. N. Studies in Mycology, Vol. 93 https://doi.org/10.1016/j.simyco.2018.06.001	journal	June 2019
A computational framework to explore large-scale biosynthetic diversity Navarro-Muñoz, Jorge C.; Selem-Mojica, Nelly; Mullowney, Michael W. Nature Chemical Biology, Vol. 16, Issue 1 https://doi.org/10.1038/s41589-019-0400-9	journal	November 2019
Beyond aflatoxin: four distinct expression patterns and functional roles associated with Aspergillus flavus secondary metabolism gene clusters Georgianna, D. Ryan; Fedorova, Natalie D.; Burroughs, James L. Molecular Plant Pathology, Vol. 11, Issue 2, p. 213-226 https://doi.org/10.1111/j.1364-3703.2009.00594.x	journal	March 2010
Latitude and Altitude Influence Secondary Metabolite Production in Peripheral Alpine Populations of the Mediterranean Species Lavandula angustifolia Mill. Demasi, Sonia; Caser, Matteo; Lonati, Michele Frontiers in Plant Science, Vol. 9 https://doi.org/10.3389/fpls.2018.00983	journal	July 2018
Recombination and local population structure of the root endophytic fungus Glutinomyces brunneus based on microsatellite analyses Nakamura, N.; Tanaka, C.; Takeuchi-Kaneko, Y. Fungal Ecology, Vol. 41 https://doi.org/10.1016/j.funeco.2019.03.009	journal	October 2019
Balancing selection for aflatoxin in Aspergillus flavus is maintained through interference competition with, and fungivory by insects Drott, Milton T.; Lazzaro, Brian P.; Brown, Dan L. Proceedings of the Royal Society B: Biological Sciences, Vol. 284, Issue 1869 https://doi.org/10.1098/rspb.2017.2408	journal	December 2017
Aspergillus texensis: A Novel Aflatoxin Producer with S Morphology from the United States Singh, Pummi; Orbach, Marc; Cotty, Peter Toxins, Vol. 10, Issue 12 https://doi.org/10.3390/toxins10120513	journal	December 2018
Identification and characterization of genes responsible for biosynthesis of kojic acid, an industrially important compound from Aspergillus oryzae Terabayashi, Yasunobu; Sano, Motoaki; Yamane, Noriko Fungal Genetics and Biology, Vol. 47, Issue 12 https://doi.org/10.1016/j.fgb.2010.08.014	journal	December 2010
Human aflatoxicosis in developing countries: a review of toxicology, exposure, potential health consequences, and interventions Williams, Jonathan H.; Phillips, Timothy D.; Jolly, Pauline E. The American Journal of Clinical Nutrition, Vol. 80, Issue 5 https://doi.org/10.1093/ajcn/80.5.1106	journal	November 2004
Synergism of aflatoxin B1 toxicity with the co-occurring fungal metabolite kojic acid to two caterpillars Dowd, Patrick F. Entomologia Experimentalis et Applicata, Vol. 47, Issue 1 https://doi.org/10.1111/j.1570-7458.1988.tb02283.x	journal	April 1988
The Evolutionary Imprint of Domestication on Genome Variation and Function of the Filamentous Fungus Aspergillus oryzae Gibbons, John G.; Salichos, Leonidas; Slot, Jason C. Current Biology, Vol. 22, Issue 15 https://doi.org/10.1016/j.cub.2012.05.033	journal	August 2012
The variant call format and VCFtools Danecek, P.; Auton, A.; Abecasis, G. Bioinformatics, Vol. 27, Issue 15 https://doi.org/10.1093/bioinformatics/btr330	journal	June 2011
Genome Sequencing and Pan-Genome Analysis of 23 Corallococcus spp. Strains Reveal Unexpected Diversity, With Particular Plasticity of Predatory Gene Sets Livingstone, Paul G.; Morphew, Russell M.; Whitworth, David E. Frontiers in Microbiology, Vol. 9 https://doi.org/10.3389/fmicb.2018.03187	journal	December 2018
Identification and functional analysis of the aspergillic acid gene cluster in Aspergillus flavus Lebar, Matthew D.; Cary, Jeffrey W.; Majumdar, Rajtilak Fungal Genetics and Biology, Vol. 116 https://doi.org/10.1016/j.fgb.2018.04.009	journal	July 2018
ggtree : an r package for visualization and annotation of phylogenetic trees with their covariates and other associated data Yu, Guangchuang; Smith, David K.; Zhu, Huachen Methods in Ecology and Evolution, Vol. 8, Issue 1 https://doi.org/10.1111/2041-210X.12628	journal	September 2016
adegenet: a R package for the multivariate analysis of genetic markers Jombart, Thibaut Bioinformatics, Vol. 24, Issue 11 https://doi.org/10.1093/bioinformatics/btn129	journal	April 2008
Comparative genomics reveals high biological diversity and specific adaptations in the industrially and medically important fungal genus Aspergillus de Vries, Ronald P.; Riley, Robert; Wiebenga, Ad Genome Biology, Vol. 18, Issue 1 https://doi.org/10.1186/s13059-017-1151-0	journal	February 2017
Complex Evolutionary Origins of Specialized Metabolite Gene Cluster Diversity among the Plant Pathogenic Fungi of the Fusarium graminearum Species Complex Tralamazza, Sabina Moser; Rocha, Liliana Oliveira; Oggenfuss, Ursula Genome Biology and Evolution, Vol. 11, Issue 11 https://doi.org/10.1093/gbe/evz225	journal	October 2019
Comparative Genomics of Pathogenic and Nonpathogenic Beetle-Vectored Fungi in the Genus Geosmithia Schuelke, Taruna A.; Wu, Guangxi; Westbrook, Anthony Genome Biology and Evolution, Vol. 9, Issue 12 https://doi.org/10.1093/gbe/evx242	journal	November 2017
Comparative genomics of geographically distant Fusarium fujikuroi isolates revealed two distinct pathotypes correlating with secondary metabolite profiles Niehaus, Eva-Maria; Kim, Hee-Kyoung; Münsterkötter, Martin PLOS Pathogens, Vol. 13, Issue 10 https://doi.org/10.1371/journal.ppat.1006670	journal	October 2017
Resolving the paradox of sex and recombination Otto, Sarah P.; Lenormand, Thomas Nature Reviews Genetics, Vol. 3, Issue 4 https://doi.org/10.1038/nrg761	journal	April 2002
Comparative genomic and transcriptomic analyses reveal the hemibiotrophic stage shift of Colletotrichum fungi Gan, Pamela; Ikeda, Kyoko; Irieda, Hiroki New Phytologist, Vol. 197, Issue 4 https://doi.org/10.1111/nph.12085	journal	December 2012
An Aspergillus flavus secondary metabolic gene cluster containing a hybrid PKS–NRPS is necessary for synthesis of the 2-pyridones, leporins Cary, Jeffrey W.; Uka, Valdet; Han, Zheng Fungal Genetics and Biology, Vol. 81 https://doi.org/10.1016/j.fgb.2015.05.010	journal	August 2015
The Aspergilli and Their Mycotoxins: Metabolic Interactions With Plants and the Soil Biota Pfliegler, Walter P.; Pócsi, István; Győri, Zoltán Frontiers in Microbiology, Vol. 10 https://doi.org/10.3389/fmicb.2019.02921	journal	February 2020
Unearthing fungal chemodiversity and prospects for drug discovery Greco, Claudio; Keller, Nancy P.; Rokas, Antonis Current Opinion in Microbiology, Vol. 51 https://doi.org/10.1016/j.mib.2019.03.002	journal	October 2019
Comparing genotype and chemotype of Fusarium graminearum from cereals in Ontario, Canada Crippin, Trinda; Renaud, Justin B.; Sumarah, Mark W. PLOS ONE, Vol. 14, Issue 5 https://doi.org/10.1371/journal.pone.0216735	journal	May 2019
The Frequency of Sex: Population Genomics Reveals Differences in Recombination and Population Structure of the Aflatoxin-Producing Fungus Aspergillus flavus Drott, Milton T.; Satterlee, Tatum R.; Skerker, Jeffrey M. mBio, Vol. 11, Issue 4 https://doi.org/10.1128/mBio.00963-20	journal	August 2020
Secondary Metabolite Dereplication and Phylogenetic Analysis Identify Various Emerging Mycotoxins and Reveal the High Intra-Species Diversity in Aspergillus flavus Uka, Valdet; Moore, Geromy G.; Arroyo-Manzanares, Natalia Frontiers in Microbiology, Vol. 10 https://doi.org/10.3389/fmicb.2019.00667	journal	April 2019
A Genomics Based Discovery of Secondary Metabolite Biosynthetic Gene Clusters in Aspergillus ustus Pi, Borui; Yu, Dongliang; Dai, Fangwei PLOS ONE, Vol. 10, Issue 2 https://doi.org/10.1371/journal.pone.0116089	journal	February 2015

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Title: Microevolution in the pansecondary metabolome of Aspergillus flavus and its potential macroevolutionary implications for filamentous fungi

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