Sexuality generates diversity in the aflatoxin gene cluster: evidence on a global scale.

Aflatoxins are produced by Aspergillus flavus and A. parasiticus in oil-rich seed and grain crops and are a serious problem in agriculture, with aflatoxin B₁ being the most carcinogenic natural compound known. Sexual reproduction in these species occurs between individuals belonging to different veg...

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Autores principales: Geromy G Moore, Jacalyn L Elliott, Rakhi Singh, Bruce W Horn, Joe W Dorner, Eric A Stone, Sofia N Chulze, German G Barros, Manjunath K Naik, Graeme C Wright, Kerstin Hell, Ignazio Carbone
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Publicado: Public Library of Science (PLoS) 2013
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Acceso en línea:https://doaj.org/article/29f50d63294c4d10ae242c7d0d223dea
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spelling oai:doaj.org-article:29f50d63294c4d10ae242c7d0d223dea2021-11-18T06:07:43ZSexuality generates diversity in the aflatoxin gene cluster: evidence on a global scale.1553-73661553-737410.1371/journal.ppat.1003574https://doaj.org/article/29f50d63294c4d10ae242c7d0d223dea2013-01-01T00:00:00Zhttps://www.ncbi.nlm.nih.gov/pmc/articles/pmid/24009506/?tool=EBIhttps://doaj.org/toc/1553-7366https://doaj.org/toc/1553-7374Aflatoxins are produced by Aspergillus flavus and A. parasiticus in oil-rich seed and grain crops and are a serious problem in agriculture, with aflatoxin B₁ being the most carcinogenic natural compound known. Sexual reproduction in these species occurs between individuals belonging to different vegetative compatibility groups (VCGs). We examined natural genetic variation in 758 isolates of A. flavus, A. parasiticus and A. minisclerotigenes sampled from single peanut fields in the United States (Georgia), Africa (Benin), Argentina (Córdoba), Australia (Queensland) and India (Karnataka). Analysis of DNA sequence variation across multiple intergenic regions in the aflatoxin gene clusters of A. flavus, A. parasiticus and A. minisclerotigenes revealed significant linkage disequilibrium (LD) organized into distinct blocks that are conserved across different localities, suggesting that genetic recombination is nonrandom and a global occurrence. To assess the contributions of asexual and sexual reproduction to fixation and maintenance of toxin chemotype diversity in populations from each locality/species, we tested the null hypothesis of an equal number of MAT1-1 and MAT1-2 mating-type individuals, which is indicative of a sexually recombining population. All samples were clone-corrected using multi-locus sequence typing which associates closely with VCG. For both A. flavus and A. parasiticus, when the proportions of MAT1-1 and MAT1-2 were significantly different, there was more extensive LD in the aflatoxin cluster and populations were fixed for specific toxin chemotype classes, either the non-aflatoxigenic class in A. flavus or the B₁-dominant and G₁-dominant classes in A. parasiticus. A mating type ratio close to 1∶1 in A. flavus, A. parasiticus and A. minisclerotigenes was associated with higher recombination rates in the aflatoxin cluster and less pronounced chemotype differences in populations. This work shows that the reproductive nature of the population (more sexual versus more asexual) is predictive of aflatoxin chemotype diversity in these agriculturally important fungi.Geromy G MooreJacalyn L ElliottRakhi SinghBruce W HornJoe W DornerEric A StoneSofia N ChulzeGerman G BarrosManjunath K NaikGraeme C WrightKerstin HellIgnazio CarbonePublic Library of Science (PLoS)articleImmunologic diseases. AllergyRC581-607Biology (General)QH301-705.5ENPLoS Pathogens, Vol 9, Iss 8, p e1003574 (2013)
institution DOAJ
collection DOAJ
language EN
topic Immunologic diseases. Allergy
RC581-607
Biology (General)
QH301-705.5
spellingShingle Immunologic diseases. Allergy
RC581-607
Biology (General)
QH301-705.5
Geromy G Moore
Jacalyn L Elliott
Rakhi Singh
Bruce W Horn
Joe W Dorner
Eric A Stone
Sofia N Chulze
German G Barros
Manjunath K Naik
Graeme C Wright
Kerstin Hell
Ignazio Carbone
Sexuality generates diversity in the aflatoxin gene cluster: evidence on a global scale.
description Aflatoxins are produced by Aspergillus flavus and A. parasiticus in oil-rich seed and grain crops and are a serious problem in agriculture, with aflatoxin B₁ being the most carcinogenic natural compound known. Sexual reproduction in these species occurs between individuals belonging to different vegetative compatibility groups (VCGs). We examined natural genetic variation in 758 isolates of A. flavus, A. parasiticus and A. minisclerotigenes sampled from single peanut fields in the United States (Georgia), Africa (Benin), Argentina (Córdoba), Australia (Queensland) and India (Karnataka). Analysis of DNA sequence variation across multiple intergenic regions in the aflatoxin gene clusters of A. flavus, A. parasiticus and A. minisclerotigenes revealed significant linkage disequilibrium (LD) organized into distinct blocks that are conserved across different localities, suggesting that genetic recombination is nonrandom and a global occurrence. To assess the contributions of asexual and sexual reproduction to fixation and maintenance of toxin chemotype diversity in populations from each locality/species, we tested the null hypothesis of an equal number of MAT1-1 and MAT1-2 mating-type individuals, which is indicative of a sexually recombining population. All samples were clone-corrected using multi-locus sequence typing which associates closely with VCG. For both A. flavus and A. parasiticus, when the proportions of MAT1-1 and MAT1-2 were significantly different, there was more extensive LD in the aflatoxin cluster and populations were fixed for specific toxin chemotype classes, either the non-aflatoxigenic class in A. flavus or the B₁-dominant and G₁-dominant classes in A. parasiticus. A mating type ratio close to 1∶1 in A. flavus, A. parasiticus and A. minisclerotigenes was associated with higher recombination rates in the aflatoxin cluster and less pronounced chemotype differences in populations. This work shows that the reproductive nature of the population (more sexual versus more asexual) is predictive of aflatoxin chemotype diversity in these agriculturally important fungi.
format article
author Geromy G Moore
Jacalyn L Elliott
Rakhi Singh
Bruce W Horn
Joe W Dorner
Eric A Stone
Sofia N Chulze
German G Barros
Manjunath K Naik
Graeme C Wright
Kerstin Hell
Ignazio Carbone
author_facet Geromy G Moore
Jacalyn L Elliott
Rakhi Singh
Bruce W Horn
Joe W Dorner
Eric A Stone
Sofia N Chulze
German G Barros
Manjunath K Naik
Graeme C Wright
Kerstin Hell
Ignazio Carbone
author_sort Geromy G Moore
title Sexuality generates diversity in the aflatoxin gene cluster: evidence on a global scale.
title_short Sexuality generates diversity in the aflatoxin gene cluster: evidence on a global scale.
title_full Sexuality generates diversity in the aflatoxin gene cluster: evidence on a global scale.
title_fullStr Sexuality generates diversity in the aflatoxin gene cluster: evidence on a global scale.
title_full_unstemmed Sexuality generates diversity in the aflatoxin gene cluster: evidence on a global scale.
title_sort sexuality generates diversity in the aflatoxin gene cluster: evidence on a global scale.
publisher Public Library of Science (PLoS)
publishDate 2013
url https://doaj.org/article/29f50d63294c4d10ae242c7d0d223dea
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