The Frequency of Sex: Population Genomics Reveals Differences in Recombination and Population Structure of the Aflatoxin-Producing Fungus Aspergillus flavus
Abstract
The apparent rarity of sex in many fungal species has raised questions about how much sex is needed to purge deleterious mutations and how differences in frequency of sex impact fungal evolution. We sought to determine how differences in the extent of recombination between populations of Aspergillus flavus impact the evolution of genes associated with the synthesis of aflatoxin, a notoriously potent carcinogen. We sequenced the genomes of, and quantified aflatoxin production in, 94 isolates of A. flavus sampled from seven states in eastern and central latitudinal transects of the United States. The overall population is subdivided into three genetically differentiated populations (A, B, and C) that differ greatly in their extent of recombination, diversity, and aflatoxin-producing ability. Estimates of the number of recombination events and linkage disequilibrium decay suggest relatively frequent sex only in population A. Population B is sympatric with population A but produces significantly less aflatoxin and is the only population where the inability of nonaflatoxigenic isolates to produce aflatoxin was explained by multiple gene deletions. Population expansion evident in population B suggests a recent introduction or range expansion. Population C is largely nonaflatoxigenic and restricted mainly to northern sampling locations through restricted migration and/or selection. Despitemore »
- Authors:
-
[1];
[4];
[1];
- Univ. of Wisconsin, Madison, WI (United States). Dept. of Medical Microbiology and Immunology
- Univ. of Wisconsin, Madison, WI (United States). Dept. of Genetics
- Univ. of California, Berkeley, CA (United States). Innovative Genomics Inst.
- Univ. of California, Berkeley, CA (United States). Innovative Genomics Inst.; Univ. of California, Berkeley, CA (United States). Dept. of Plant and Microbial Biology; Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Environmental Genomics and Systems Biology
- Cornell Univ., Ithaca, NY (United States). School of Integrative Plant Science. Plant Pathology and Plant-Microbe Biology Section
- Publication Date:
- Research Org.:
- Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC)
- OSTI Identifier:
- 1816101
- Grant/Contract Number:
- AC02-05CH11231
- Resource Type:
- Accepted Manuscript
- Journal Name:
- mBio
- Additional Journal Information:
- Journal Volume: 11; Journal Issue: 4; Journal ID: ISSN 2161-2129
- Publisher:
- American Society for Microbiology (ASM)
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; Aspergillus flavus; sex; recombination; aflatoxin; population structure; population genomics
Citation Formats
Drott, Milton T., Satterlee, Tatum R., Skerker, Jeffrey M., Pfannenstiel, Brandon T., Glass, N. Louise, Keller, Nancy P., and Milgroom, Michael G. The Frequency of Sex: Population Genomics Reveals Differences in Recombination and Population Structure of the Aflatoxin-Producing Fungus Aspergillus flavus. United States: N. p., 2020.
Web. doi:10.1128/mBio.00963-20.
Drott, Milton T., Satterlee, Tatum R., Skerker, Jeffrey M., Pfannenstiel, Brandon T., Glass, N. Louise, Keller, Nancy P., & Milgroom, Michael G. The Frequency of Sex: Population Genomics Reveals Differences in Recombination and Population Structure of the Aflatoxin-Producing Fungus Aspergillus flavus. United States. https://doi.org/10.1128/mBio.00963-20
Drott, Milton T., Satterlee, Tatum R., Skerker, Jeffrey M., Pfannenstiel, Brandon T., Glass, N. Louise, Keller, Nancy P., and Milgroom, Michael G. Tue .
"The Frequency of Sex: Population Genomics Reveals Differences in Recombination and Population Structure of the Aflatoxin-Producing Fungus Aspergillus flavus". United States. https://doi.org/10.1128/mBio.00963-20. https://www.osti.gov/servlets/purl/1816101.
@article{osti_1816101,
title = {The Frequency of Sex: Population Genomics Reveals Differences in Recombination and Population Structure of the Aflatoxin-Producing Fungus Aspergillus flavus},
author = {Drott, Milton T. and Satterlee, Tatum R. and Skerker, Jeffrey M. and Pfannenstiel, Brandon T. and Glass, N. Louise and Keller, Nancy P. and Milgroom, Michael G.},
abstractNote = {The apparent rarity of sex in many fungal species has raised questions about how much sex is needed to purge deleterious mutations and how differences in frequency of sex impact fungal evolution. We sought to determine how differences in the extent of recombination between populations of Aspergillus flavus impact the evolution of genes associated with the synthesis of aflatoxin, a notoriously potent carcinogen. We sequenced the genomes of, and quantified aflatoxin production in, 94 isolates of A. flavus sampled from seven states in eastern and central latitudinal transects of the United States. The overall population is subdivided into three genetically differentiated populations (A, B, and C) that differ greatly in their extent of recombination, diversity, and aflatoxin-producing ability. Estimates of the number of recombination events and linkage disequilibrium decay suggest relatively frequent sex only in population A. Population B is sympatric with population A but produces significantly less aflatoxin and is the only population where the inability of nonaflatoxigenic isolates to produce aflatoxin was explained by multiple gene deletions. Population expansion evident in population B suggests a recent introduction or range expansion. Population C is largely nonaflatoxigenic and restricted mainly to northern sampling locations through restricted migration and/or selection. Despite differences in the number and type of mutations in the aflatoxin gene cluster, codon optimization and site frequency differences in synonymous and nonsynonymous mutations suggest that low levels of recombination in some A. flavus populations are sufficient to purge deleterious mutations.},
doi = {10.1128/mBio.00963-20},
journal = {mBio},
number = 4,
volume = 11,
place = {United States},
year = {Tue Jul 14 00:00:00 EDT 2020},
month = {Tue Jul 14 00:00:00 EDT 2020}
}
Free Publicly Available Full Text
Publisher's Version of Record
Other availability
Search WorldCat to find libraries that may hold this journal
Save to My Library
You must Sign In or Create an Account in order to save documents to your library.
Works referenced in this record:
NEUROSPORA AND THE DEAD-END HYPOTHESIS: GENOMIC CONSEQUENCES OF SELFING IN THE MODEL GENUS: GENOMIC MALADAPTATION IN SELFING FUNGAL SPECIES
journal, August 2013
- Gioti, Anastasia; Stajich, Jason E.; Johannesson, Hanna
- Evolution, Vol. 67, Issue 12
QUAST: quality assessment tool for genome assemblies
journal, February 2013
- Gurevich, Alexey; Saveliev, Vladislav; Vyahhi, Nikolay
- Bioinformatics, Vol. 29, Issue 8
Vegetative Compatibility within Populations of Aspergillus flavus, A. parasiticus, and A. tamarii from a Peanut Field
journal, May 1995
- Horn, Bruce W.; Greene, Ronald L.
- Mycologia, Vol. 87, Issue 3
Sequence breakpoints in the aflatoxin biosynthesis gene cluster and flanking regions in nonaflatoxigenic Aspergillus flavus isolates
journal, November 2005
- Chang, Perng-Kuang; Horn, Bruce W.; Dorner, Joe W.
- Fungal Genetics and Biology, Vol. 42, Issue 11
Recombination and the Multilocus Structure of Fungal Populations
journal, September 1996
- Milgroom, Michael G.
- Annual Review of Phytopathology, Vol. 34, Issue 1
Sexual reproduction in Aspergillus flavus
journal, May 2009
- Horn, Bruce W.; Moore, Geromy G.; Carbone, Ignazio
- Mycologia, Vol. 101, Issue 3
Mathematical model for studying genetic variation in terms of restriction endonucleases.
journal, October 1979
- Nei, M.; Li, W. H.
- Proceedings of the National Academy of Sciences, Vol. 76, Issue 10
Molecular mechanisms of Aspergillus flavus secondary metabolism and development
journal, May 2014
- Amare, Meareg G.; Keller, Nancy P.
- Fungal Genetics and Biology, Vol. 66
The ade4 Package: Implementing the Duality Diagram for Ecologists
journal, January 2007
- Dray, Stéphane; Dufour, Anne-Béatrice
- Journal of Statistical Software, Vol. 22, Issue 4
Sexual Reproduction in Aspergillus flavus Sclerotia Naturally Produced in Corn
journal, January 2014
- Horn, Bruce W.; Sorensen, Ronald B.; Lamb, Marshall C.
- Phytopathology®, Vol. 104, Issue 1
The frequency of sex in fungi
journal, October 2016
- Nieuwenhuis, Bart P. S.; James, Timothy Y.
- Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 371, Issue 1706
The Phylogenetics of Mycotoxin and Sclerotium Production in Aspergillus flavus and Aspergillus oryzae
journal, December 2000
- Geiser, David M.; Dorner, Joe W.; Horn, Bruce W.
- Fungal Genetics and Biology, Vol. 31, Issue 3
Soil Populations of Aspergillus Species from Section Flavi along a Transect through Peanut-Growing Regions of the United States
journal, September 1998
- Horn, B. W.; Dorner, J. W.
- Mycologia, Vol. 90, Issue 5
Sex, outcrossing and mating types: unsolved questions in fungi and beyond: Sexy fungi
journal, April 2012
- Billiard, S.; LÓPez-Villavicencio, M.; Hood, M. E.
- Journal of Evolutionary Biology, Vol. 25, Issue 6
Integrative analyses reveal transcriptome-proteome correlation in biological pathways and secondary metabolism clusters in A. flavus in response to temperature
journal, September 2015
- Bai, Youhuang; Wang, Sen; Zhong, Hong
- Scientific Reports, Vol. 5, Issue 1
Fast and accurate short read alignment with Burrows-Wheeler transform
journal, May 2009
- Li, H.; Durbin, R.
- Bioinformatics, Vol. 25, Issue 14
Adaptive protein evolution at the Adh locus in Drosophila
journal, June 1991
- McDonald, John H.; Kreitman, Martin
- Nature, Vol. 351, Issue 6328
Vegetative compatibility and genetic diversity in the Aspergillus flavus population of a single field
journal, August 1991
- Bayman, Paul; Cotty, Peter J.
- Canadian Journal of Botany, Vol. 69, Issue 8
Estimating the number of sexual events per generation in a facultatively sexual haploid population
journal, December 2018
- Ennos, Richard A.; Hu, Xin-Sheng
- Heredity, Vol. 122, Issue 6
Structure of an Aspergillus flavus population from maize kernels in northern Italy
journal, March 2013
- Mauro, Antonio; Battilani, Paola; Callicott, Kenneth A.
- International Journal of Food Microbiology, Vol. 162, Issue 1
PLINK: A Tool Set for Whole-Genome Association and Population-Based Linkage Analyses
journal, September 2007
- Purcell, Shaun; Neale, Benjamin; Todd-Brown, Kathe
- The American Journal of Human Genetics, Vol. 81, Issue 3
Poppr : an R package for genetic analysis of populations with clonal, partially clonal, and/or sexual reproduction
journal, January 2014
- Kamvar, Zhian N.; Tabima, Javier F.; Grünwald, Niklaus J.
- PeerJ, Vol. 2
Population Subdivision and the Frequency of Aflatoxigenic Isolates in Aspergillus flavus in the United States
journal, May 2019
- Drott, Milton T.; Fessler, Lauren M.; Milgroom, Michael G.
- Phytopathology®, Vol. 109, Issue 5
Genomics of Aspergillus oryzae: Learning from the History of Koji Mold and Exploration of Its Future
journal, May 2008
- Machida, M.; Yamada, O.; Gomi, K.
- DNA Research, Vol. 15, Issue 4
Biocontrol Strains Differentially Shift the Genetic Structure of Indigenous Soil Populations of Aspergillus flavus
journal, July 2019
- Lewis, Mary H.; Carbone, Ignazio; Luis, Jane M.
- Frontiers in Microbiology, Vol. 10
Statistical method for testing the neutral mutation hypothesis by DNA polymorphism.
journal, November 1989
- Tajima, F.
- Genetics, Vol. 123, Issue 3
Clonal reproduction in fungi
journal, July 2015
- Taylor, John W.; Hann-Soden, Christopher; Branco, Sara
- Proceedings of the National Academy of Sciences, Vol. 112, Issue 29
AUGUSTUS: a web server for gene prediction in eukaryotes that allows user-defined constraints
journal, July 2005
- Stanke, M.; Morgenstern, B.
- Nucleic Acids Research, Vol. 33, Issue Web Server
Detection of sharing by descent, long-range phasing and haplotype imputation
journal, August 2008
- Kong, Augustine; Masson, Gisli; Frigge, Michael L.
- Nature Genetics, Vol. 40, Issue 9
Comparative Population Genomics Analysis of the Mammalian Fungal Pathogen Pneumocystis
journal, July 2018
- Cissé, Ousmane H.; Ma, Liang; Wei Huang, Da
- mBio, Vol. 9, Issue 3
Regional Differences in Production of Aflatoxin B 1 and Cyclopiazonic Acid by Soil Isolates of Aspergillus flavus along a Transect within the United States
journal, April 1999
- Horn, B. W.; Dorner, J. W.
- Applied and Environmental Microbiology, Vol. 65, Issue 4
Fitness Cost of Aflatoxin Production in Aspergillus flavus When Competing with Soil Microbes Could Maintain Balancing Selection
journal, February 2019
- Drott, Milton T.; Debenport, Tracy; Higgins, Steven A.
- mBio, Vol. 10, Issue 1
Global Burden of Aflatoxin-Induced Hepatocellular Carcinoma: A Risk Assessment
journal, June 2010
- Liu, Yan; Wu, Felicia
- Environmental Health Perspectives, Vol. 118, Issue 6
The epigenetic reader SntB regulates secondary metabolism, development and global histone modifications in Aspergillus flavus
journal, November 2018
- Pfannenstiel, Brandon T.; Greco, Claudio; Sukowaty, Andrew T.
- Fungal Genetics and Biology, Vol. 120
Aflatoxin Exposure in Developing Countries: The Critical Interface of Agriculture and Health
journal, June 2007
- Wild, Christopher Paul
- Food and Nutrition Bulletin, Vol. 28, Issue 2_suppl2
Recombination between Clonal Lineages of the Asexual Fungus Verticillium dahliae Detected by Genotyping by Sequencing
journal, September 2014
- Milgroom, Michael G.; Jiménez-Gasco, María del Mar; Olivares García, Concepción
- PLoS ONE, Vol. 9, Issue 9
Evolvability of an Optimal Recombination Rate
journal, December 2015
- Lobkovsky, Alexander E.; Wolf, Yuri I.; Koonin, Eugene V.
- Genome Biology and Evolution, Vol. 8, Issue 1
Challenges facing the biological control strategy for eliminating aflatoxin contamination
journal, January 2015
- Ehrlich, K. C.; Moore, G. G.; Mellon, J. E.
- World Mycotoxin Journal, Vol. 8, Issue 2
The Current Epidemic of the Barley Pathogen Ramularia collo-cygni Derives from a Population Expansion and Shows Global Admixture
journal, December 2019
- Stam, Remco; Sghyer, Hind; Tellier, Aurélien
- Phytopathology®, Vol. 109, Issue 12
Cryptic speciation and recombination in the aflatoxin-producing fungus Aspergillus flavus
journal, January 1998
- Geiser, D. M.; Pitt, J. I.; Taylor, J. W.
- Proceedings of the National Academy of Sciences, Vol. 95, Issue 1
RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies
journal, January 2014
- Stamatakis, Alexandros
- Bioinformatics, Vol. 30, Issue 9
Population genomics of the wild yeast Saccharomyces paradoxus: Quantifying the life cycle
journal, March 2008
- Tsai, I. J.; Bensasson, D.; Burt, A.
- Proceedings of the National Academy of Sciences, Vol. 105, Issue 12
TASSEL: software for association mapping of complex traits in diverse samples
journal, June 2007
- Bradbury, P. J.; Zhang, Z.; Kroon, D. E.
- Bioinformatics, Vol. 23, Issue 19
Sexual reproduction and recombination in the aflatoxin-producing fungus Aspergillus parasiticus
journal, February 2009
- Horn, Bruce W.; Ramirez-Prado, Jorge H.; Carbone, Ignazio
- Fungal Genetics and Biology, Vol. 46, Issue 2
SPAdes: A New Genome Assembly Algorithm and Its Applications to Single-Cell Sequencing
journal, May 2012
- Bankevich, Anton; Nurk, Sergey; Antipov, Dmitry
- Journal of Computational Biology, Vol. 19, Issue 5
Whole-genome sequencing reveals recent and frequent genetic recombination between clonal lineages of Cryphonectria parasitica in western Europe
journal, September 2019
- Demené, Arthur; Legrand, Ludovic; Gouzy, Jérôme
- Fungal Genetics and Biology, Vol. 130
Degeneration of aflatoxin gene clusters in Aspergillus flavus from Africa and North America
journal, August 2016
- Adhikari, Bishwo N.; Bandyopadhyay, Ranajit; Cotty, Peter J.
- AMB Express, Vol. 6, Issue 1
The Population Genetics of Clonal and Partially Clonal Diploids
journal, August 2003
- Balloux, François; Lehmann, Laurent; de Meeûs, Thierry
- Genetics, Vol. 164, Issue 4
Clonal population structure of the chestnut blight fungus in expanding ranges in southeastern Europe
journal, October 2008
- Milgroom, Michael G.; Sotirovski, Kiril; Spica, Domenico
- Molecular Ecology, Vol. 17, Issue 20
A High-Definition View of Functional Genetic Variation from Natural Yeast Genomes
journal, January 2014
- Bergström, Anders; Simpson, Jared T.; Salinas, Francisco
- Molecular Biology and Evolution, Vol. 31, Issue 4
Taxonomy of Aspergillus section Flavi and their production of aflatoxins, ochratoxins and other mycotoxins
journal, June 2019
- Frisvad, J. C.; Hubka, V.; Ezekiel, C. N.
- Studies in Mycology, Vol. 93
Genetic diversity in Aspergillus flavus : association with aflatoxin production and morphology
journal, January 1993
- Bayman, Paul; Cotty, Peter J.
- Canadian Journal of Botany, Vol. 71, Issue 1
The Genome Analysis Toolkit: A MapReduce framework for analyzing next-generation DNA sequencing data
journal, July 2010
- McKenna, A.; Hanna, M.; Banks, E.
- Genome Research, Vol. 20, Issue 9
Balancing selection for aflatoxin in Aspergillus flavus is maintained through interference competition with, and fungivory by insects
journal, December 2017
- Drott, Milton T.; Lazzaro, Brian P.; Brown, Dan L.
- Proceedings of the Royal Society B: Biological Sciences, Vol. 284, Issue 1869
Aspergillus texensis: A Novel Aflatoxin Producer with S Morphology from the United States
journal, December 2018
- Singh, Pummi; Orbach, Marc; Cotty, Peter
- Toxins, Vol. 10, Issue 12
Human aflatoxicosis in developing countries: a review of toxicology, exposure, potential health consequences, and interventions
journal, November 2004
- Williams, Jonathan H.; Phillips, Timothy D.; Jolly, Pauline E.
- The American Journal of Clinical Nutrition, Vol. 80, Issue 5
The variant call format and VCFtools
journal, June 2011
- Danecek, P.; Auton, A.; Abecasis, G.
- Bioinformatics, Vol. 27, Issue 15
The Evolutionary Imprint of Domestication on Genome Variation and Function of the Filamentous Fungus Aspergillus oryzae
journal, August 2012
- Gibbons, John G.; Salichos, Leonidas; Slot, Jason C.
- Current Biology, Vol. 22, Issue 15
adegenet: a R package for the multivariate analysis of genetic markers
journal, April 2008
- Jombart, Thibaut
- Bioinformatics, Vol. 24, Issue 11
Virulence and isozyme diversity of sexual versus asexual collections of Uromyces appendiculatus (bean rust fungus)
journal, September 1995
- Groth, James V.; McCain, John W.; Roelfs, Alan P.
- Heredity, Vol. 75, Issue 3
ClonalFrameML: Efficient Inference of Recombination in Whole Bacterial Genomes
journal, February 2015
- Didelot, Xavier; Wilson, Daniel J.
- PLOS Computational Biology, Vol. 11, Issue 2
SplitsTree: analyzing and visualizing evolutionary data
journal, February 1998
- Huson, D. H.
- Bioinformatics, Vol. 14, Issue 1
Some Genetic Aspects of Sex
journal, March 1932
- Muller, H. J.
- The American Naturalist, Vol. 66, Issue 703
T HE E VOLUTION OF A SEXUAL F UNGI : Reproduction, Speciation and Classification
journal, September 1999
- Taylor, Jw; Jacobson, Dj; Fisher, Mc
- Annual Review of Phytopathology, Vol. 37, Issue 1
BUSCO Applications from Quality Assessments to Gene Prediction and Phylogenomics
journal, December 2017
- Waterhouse, Robert M.; Seppey, Mathieu; Simão, Felipe A.
- Molecular Biology and Evolution, Vol. 35, Issue 3
A program for annotating and predicting the effects of single nucleotide polymorphisms, SnpEff: SNPs in the genome of Drosophila melanogaster strain w
journal, April 2012
- Cingolani, Pablo; Platts, Adrian; Wang, Le Lily
- Fly, Vol. 6, Issue 2