Population-specific transcriptomic shifts underlie secondary metabolic diversification in Aspergillus flavus Link and the domestication of Aspergillus oryzae (Ahlb.).
9 affiliations
- 1U.S. Department of Agriculture-Agricultural Research Service, Cereal Disease Laboratory, St. Paul, MN 55108, USA U.S. Department of Agriculture-Agricultural Research Service, Cereal Disease Laboratory St. Paul United States of America https://ror.org/04fx69j13.
- 2Department of Biostatistics, Yale School of Public Health, New Haven, CT, USA Department of Biostatistics, Yale School of Public Health New Haven United States of America.
- 3Department of Plant Pathology, University of Georgia, Athens, GA, USA Department of Plant Pathology, University of Georgia Athens United States of America https://ror.org/00te3t702.
- 4Department of Medical Microbiology and Immunology, University of Wisconsin-Madison, Madison, WI, USA Department of Medical Microbiology and Immunology, University of Wisconsin-Madison Madison United States of America https://ror.org/01y2jtd41.
- 5U.S. Department of Agriculture-Agricultural Research Service, Food Quality Laboratory, Beltsville, MD, USA U.S. Department of Agriculture-Agricultural Research Service, Food Quality Laboratory Beltsville United States of America.
- 6Department of Bacteriology, University of Wisconsin, Madison, WI, USA Department of Bacteriology, University of Wisconsin Madison United States of America https://ror.org/01y2jtd41.
- 7Department of Biological Sciences, Vanderbilt University, Nashville, TN, USA Department of Biological Sciences, Vanderbilt University Nashville United States of America.
- 8Department of Food Science, College of Natural Sciences, University of Massachusetts Amherst, Amherst, Massachusetts, USA Department of Food Science, College of Natural Sciences, University of Massachusetts Amherst Amherst United States of America https://ror.org/0072zz521.
- 9Department of Plant Pathology, University of Wisconsin, Madison, WI, USA Department of Plant Pathology, University of Wisconsin Madison United States of America https://ror.org/01y2jtd41.
Abstract
The genomic signatures of microbial domestication remain poorly understood within the context of natural population variation. Here, we demonstrate that Aspergillus oryzae , the filamentous fungus used in soy sauce and sake production, shares more recent ancestry with a predominantly northern, largely non-aflatoxigenic population of Aspergillus flavus (population C). A. oryzae isolates also overlap with the recently described, clinically enriched A. flavus population D, suggesting multiple domestication events. All isolates tested retained pathogenicity in a zebrafish infection model. At the transcriptomic level, populations are significantly differentiated and respond differently to spore density, suggesting population-specific adaptations to ecological conditions. Although most transcriptomic variation was consistent with phylogenetic relationships, several co-expression modules exhibited significantly greater divergence than expected from phylogeny alone, suggesting that phenotypic diversification may sometimes occur through the reorganization of transcriptomic architectures. A. oryzae also displayed elevated expression of a carbohydrate-metabolism module; however, this pattern was consistent with phylogenetic differentiation, suggesting that enhanced carbohydrate metabolism may have begun evolving prior to domestication or may be most apparent under fermentation-relevant conditions. Population-specific variation is also evident among secondary metabolite (SM) gene clusters. While A. oryzae shows markedly reduced expression of aflatoxin biosynthesis genes, this trend does not extend across the entire secondary metabolome. Using machine-learning-based gene regulatory network inference, we identified population-specific transcriptomic differences linked to distinct transcription factors, with evidence for both cis- and trans-acting regulatory divergence, but no changes in global regulators such as laeA . Together, these findings provide new insights into the domestication of A. oryzae , its global significance, and the microevolution of fungal secondary metabolic pathways.
Related
- Integrated Physiological and Transcriptomic Analyses Reveal Secondary Metabolic Responses of Prunella vulgaris Seedlings to Sodium Nitroprusside Treatment
- Taming wild replicons: evolution and domestication of large extrachromosomal replicons
- Genomic Tales of Wine Yeasts: From Domestication to Functional Innovation
- A spatiotemporal single‐cell atlas of porcine development reveals regulatory dynamics and cellular targets of domestication
- A Systematic Method for Analysing Germination of Aspergillus Conidia Using Real‐Time Imaging
BibTeX
@article{drott2026populationspecific,
title = {{Population-specific transcriptomic shifts underlie secondary metabolic diversification in Aspergillus flavus Link and the domestication of Aspergillus oryzae (Ahlb.).}},
author = {Milton T Drott and Yen-Wen Wang and E Anne Hatmaker and Nayanna M Mercado-Soto and J Mitch Elmore and Dianiris Luciano-Rosaro and Jae-Hyuk Yu and Antonis Rokas and John G Gibbons and Anna Huttenlocher and Kunlong Yang and Nancy P Keller},
journal = {IMA fungus},
year = {2026},
month = oct,
doi = {10.3897/imafungus.17.195218},
url = {https://europepmc.org/article/MED/42889696},
note = {Public domain},
}
RIS
TY - JOUR
TI - Population-specific transcriptomic shifts underlie secondary metabolic diversification in Aspergillus flavus Link and the domestication of Aspergillus oryzae (Ahlb.).
AU - Milton T Drott
AU - Yen-Wen Wang
AU - E Anne Hatmaker
AU - Nayanna M Mercado-Soto
AU - J Mitch Elmore
AU - Dianiris Luciano-Rosaro
AU - Jae-Hyuk Yu
AU - Antonis Rokas
AU - John G Gibbons
AU - Anna Huttenlocher
AU - Kunlong Yang
AU - Nancy P Keller
PY - 2026
DA - 2026/10/07
JO - IMA fungus
DO - 10.3897/imafungus.17.195218
UR - https://europepmc.org/article/MED/42889696
AB - The genomic signatures of microbial domestication remain poorly understood within the context of natural population variation. Here, we demonstrate that Aspergillus oryzae , the filamentous fungus used in soy sauce and sake production, shares more recent ancestry with a predominantly northern, largely non-aflatoxigenic population of Aspergillus flavus (population C). A. oryzae isolates also overlap with the recently described, clinically enriched A. flavus population D, suggesting multiple domestication events. All isolates tested retained pathogenicity in a zebrafish infection model. At the transcriptomic level, populations are significantly differentiated and respond differently to spore density, suggesting population-specific adaptations to ecological conditions. Although most transcriptomic variation was consistent with phylogenetic relationships, several co-expression modules exhibited significantly greater divergence than expected from phylogeny alone, suggesting that phenotypic diversification may sometimes occur through the reorganization of transcriptomic architectures. A. oryzae also displayed elevated expression of a carbohydrate-metabolism module; however, this pattern was consistent with phylogenetic differentiation, suggesting that enhanced carbohydrate metabolism may have begun evolving prior to domestication or may be most apparent under fermentation-relevant conditions. Population-specific variation is also evident among secondary metabolite (SM) gene clusters. While A. oryzae shows markedly reduced expression of aflatoxin biosynthesis genes, this trend does not extend across the entire secondary metabolome. Using machine-learning-based gene regulatory network inference, we identified population-specific transcriptomic differences linked to distinct transcription factors, with evidence for both cis- and trans-acting regulatory divergence, but no changes in global regulators such as laeA . Together, these findings provide new insights into the domestication of A. oryzae , its global significance, and the microevolution of fungal secondary metabolic pathways.
SN - 2210-6340
SN - 2210-6359
ER -