Journal Article

Aspergillus flavus pangenome (AflaPan) uncovers novel aflatoxin and secondary metabolite associated gene clusters

Pandey, Manish K., Gangurde, Sunil S., Holbrook, C. Corley, Wang, Hui, Korani, Walid, Fountain, Jake C., Agarwal, Gaurav, Dutta, Bhabesh, Chang, Perng-Kuang, Bajaj, Prasad, Abbas, Hamed K., Varshney, Rajeev K., Guo, Baozhu, Clevenger, Josh P., Kemerait, Robert C.

2024

Overview

Background Aspergillus flavus is an important agricultural and food safety threat due to its production of carcinogenic aflatoxins. It has high level of genetic diversity that is adapted to various environments. Recently, we reported two reference genomes of A. flavus isolates, AF13 ( MAT1-2 and highly aflatoxigenic isolate) and NRRL3357 ( MAT1-1 and moderate aflatoxin producer). Where, an insertion of 310 kb in AF13 included an aflatoxin producing gene bZIP transcription factor, named atfC . Observations of significant genomic variants between these isolates of contrasting phenotypes prompted an investigation into variation among other agricultural isolates of A. flavus with the goal of discovering novel genes potentially associated with aflatoxin production regulation. Present study was designed with three main objectives: (1) collection of large number of A. flavus isolates from diverse sources including maize plants and field soils; (2) whole genome sequencing of collected isolates and development of a pangenome; and (3) pangenome-wide association study (Pan-GWAS) to identify novel secondary metabolite cluster genes. Results Pangenome analysis of 346 A. flavus isolates identified a total of 17,855 unique orthologous gene clusters, with mere 41% (7,315) core genes and 59% (10,540) accessory genes indicating accumulation of high genomic diversity during domestication. 5,994 orthologous gene clusters in accessory genome not annotated in either the A. flavus AF13 or NRRL3357 reference genomes. Pan-genome wide association analysis of the genomic variations identified 391 significant associated pan-genes associated with aflatoxin production. Interestingly, most of the significantly associated pan-genes (94%; 369 associations) belonged to accessory genome indicating that genome expansion has resulted in the incorporation of new genes associated with aflatoxin and other secondary metabolites. Conclusion In summary, this study provides complete pangenome framework for the species of Aspergillus flavus along with associated genes for pathogen survival and aflatoxin production. The large accessory genome indicated large genome diversity in the species A. flavus , however AflaPan is a closed pangenome represents optimum diversity of species A. flavus . Most importantly, the newly identified aflatoxin producing gene clusters will be a new source for seeking aflatoxin mitigation strategies and needs new attention in research.

• Publisher: BioMed Central,BioMed Central Ltd,Springer Nature B.V,BMC
• Subject: Accessory genome / Aflatoxin / Aflatoxins / Aflatoxins - genetics / Aflatoxins - metabolism / Agriculture / Analysis / Aspergillus / Aspergillus flavus / Aspergillus flavus - genetics / Aspergillus flavus - metabolism / Association analysis / Biological diversity / Biomedical and Life Sciences / carcinogenicity / Carcinogens / Clusters / Core genome / corn / DNA sequencing / Domestication / Ethylenediaminetetraacetic acid / Food / Food safety / Gene clusters / Gene sequencing / Genes / Genes, Fungal / Genetic aspects / Genetic diversity / Genetic research / Genetic transcription / Genetic Variation / genome expansion / Genome, Fungal / Genome-Wide Association Study / Genomes / Genomic analysis / Genomic diversity / Genomics / Life Sciences / Metabolites / Multi-omics approaches for plant disease diagnosis / Multigene Family / Nucleotide sequencing / Oxidative stress / pan-GWAS / pathogen survival / Pathogens / Phenotypes / Physiological aspects / Plant metabolites / Plant Sciences / Safety and security measures / Secondary Metabolism - genetics / Secondary metabolites / Soils / species / Species diversity / Transcription factors / Tree Biology / Whole Genome Sequencing / Zea mays - genetics / Zea mays - microbiology