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United States Department of Agriculture

Agricultural Research Service

Research Project: CONTROL MECHANISMS FOR MYCOTOXIN PREVENTION IN PEANUTS AND THEIR ROTATION CROPS

Location: Peanut Research

Title: Effect of sexual recombination on population diversity in aflatoxin production by Aspergillus flavus and evidence for cryptic heterokaryosis

Authors
item Olarte, Rodrigo -
item Horn, Bruce
item Dorner, Joe -
item Monacell, James -
item Singh, Rahkhi -
item Stone, Eric -
item Carbone, Ignazio -

Submitted to: Molecular Ecology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: October 19, 2011
Publication Date: March 6, 2012
Citation: Olarte, R.A., Horn, B.W., Dorner, J.W., Monacell, J.T., Singh, R., Stone, E.A., Carbone, I. 2012. Effect of sexual recombination on population diversity in aflatoxin production by Aspergillus flavus and evidence for cryptic heterokaryosis. Molecular Ecology. 21:1453-1476..

Interpretive Summary: Aspergillus flavus is the major producer of aflatoxins, which are potent carcinogens. Outbreaks of human aflatoxicosis occur in regions where highly contaminated food is ingested; for example, in Kenya, East Africa, in 2004, 125 people died from an aflatoxin outbreak. Over 100 countries have stringent regulatory limits on allowable concentrations in human and animal foods. Over a billion dollars is lost annually from mycotoxin contamination of agricultural commodities, notably maize, peanuts, and cottonseed, and many millions more are spent on regulation and control. A. flavus is also an emerging human pathogen that is second only to A. fumigatus as a leading cause of Aspergillosis. In the present study, we provide direct genetic evidence from experimental and natural populations to show that sex not only plays an integral role in the life history of this fungus, but also is responsible for genetic diversity in aflatoxin production. We also report for the first time in this fungus the presence of genetic material in sexual progeny that could not be detected in the parents. Our results have significant implications for managing aflatoxin contamination of crops and for improving biocontrol strategies using non-aflatoxigenic strains of A. flavus.

Technical Abstract: Aspergillus flavus is the major producer of carcinogenic aflatoxins (AFs) in crops worldwide. Natural populations of A. flavus show tremendous variation in AF production, some of which can be attributed to environmental conditions, differential regulation of the AF biosynthetic pathway, and deletions or loss-of-function mutations in the AF gene cluster. Understanding the evolutionary processes that generate genetic diversity in A. flavus may also explain quantitative differences in aflatoxigenicity. Several population studies using multilocus genealogical approaches provide indirect evidence of recombination in the genome and specifically in the AF gene cluster. More recently, A. flavus has been shown to be functionally heterothallic and capable of sexual reproduction in laboratory crosses. In the present study, we characterize the progeny from nine A. flavus crosses using toxin phenotype assays, DNA sequence-based markers and array comparative genome hybridization. We show high AF heritability linked to genetic variation in the AF gene cluster, as well as recombination through the independent assortment of chromosomes and through crossing over within the AF cluster that coincides with inferred recombination blocks and hotspots in natural populations. Moreover, the vertical transmission of cryptic alleles indicates that while an A. flavus deletion strain is predominantly homokaryotic, it may harbor AF cluster genes at a low copy number. Results from experimental matings indicate that sexual recombination is driving genetic and functional hyperdiversity in A. flavus. The results of this study have significant implications for managing AF contamination of crops and for improving biocontrol strategies using nonaflatoxigenic strains of A. flavus.Aspergillus flavus is the major producer of carcinogenic aflatoxins (AFs) in crops worldwide. Natural populations of A. flavus show tremendous variation in AF production, some of which can be attributed to environmental conditions, differential regulation of the AF biosynthetic pathway, and deletions or loss-of-function mutations in the AF gene cluster. Understanding the evolutionary processes that generate genetic diversity in A. flavus may also explain quantitative differences in aflatoxigenicity. Several population studies using multilocus genealogical approaches provide indirect evidence of recombination in the genome and specifically in the AF gene cluster. More recently, A. flavus has been shown to be functionally heterothallic and capable of sexual reproduction in laboratory crosses. In the present study, we characterize the progeny from nine A. flavus crosses using toxin phenotype assays, DNA sequence-based markers and array comparative genome hybridization. We show high AF heritability linked to genetic variation in the AF gene cluster, as well as recombination through the independent assortment of chromosomes and through crossing over within the AF cluster that coincides with inferred recombination blocks and hotspots in natural populations. Moreover, the vertical transmission of cryptic alleles indicates that while an A. flavus deletion strain is predominantly homokaryotic, it may harbor AF cluster genes at a low copy number. Results from experimental matings indicate that sexual recombination is driving genetic and functional hyperdiversity in A. flavus. The results of this study have significant implications for managing AF contamination of crops and for improving biocontrol strategies using nonaflatoxigenic strains of A. flavus.

Last Modified: 4/18/2014
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