Accessory Chromosome-Acquired Secondary Metabolism in Plant Pathogenic Fungi: The Evolution of Biotrophs Into
Thomas E Witte1,2, Nicolas Villeneuve1,2, Christopher N Boddy2
1Agriculture and Agri-Food Canada, Ottawa Research and Development Centre, Ottawa, ON, Canada.
Abstract:
Accessory chromosomes are strain- or pathotype-specific chromosomes that exist in addition to the core chromosomes of a species and are generally not considered essential to the survival of the organism. Among pathogenic fungal species, accessory chromosomes harbor pathogenicity or virulence factor genes, several of which are known to encode for secondary metabolites that are involved in plant tissue invasion. Accessory chromosomes are of particular interest due to their capacity for horizontal transfer between strains and their dynamic "crosstalk" with core chromosomes. This review focuses exclusively on secondary metabolism (including mycotoxin biosynthesis) associated with accessory chromosomes in filamentous fungi and the role accessory chromosomes play in the evolution of secondary metabolite gene clusters. Untargeted metabolomics profiling in conjunction with genome sequencing provides an effective means of linking secondary metabolite products with their respective biosynthetic gene clusters that reside on accessory chromosomes. While the majority of literature describing accessory chromosome-associated toxin biosynthesis comes from studies of Alternaria pathotypes, the recent discovery of accessory chromosome-associated biosynthetic genes in Fusarium species offer fresh insights into the evolution of biosynthetic enzymes such as non-ribosomal peptide synthetases (NRPSs), polyketide synthases (PKSs) and regulatory mechanisms governing their expression.
Insights
Filamentous fungi accessory chromosomes carry virulence genes, influencing plant invasion and toxin production. Their horizontal transfer and interaction with core chromosomes drive the evolution of secondary metabolite gene clusters.
Area of Science:
- Mycology
- Genomics
- Biochemistry
Background:
- Accessory chromosomes are non-essential, strain-specific DNA elements in fungi.
- These chromosomes often harbor genes for pathogenicity and secondary metabolites, including mycotoxins.
- Accessory chromosomes are known for horizontal transfer and interaction with core genomes.
Purpose of the Study:
- To review secondary metabolism, including mycotoxin biosynthesis, on accessory chromosomes in filamentous fungi.
- To explore the role of accessory chromosomes in the evolution of secondary metabolite gene clusters.
- To highlight the utility of integrating metabolomics and genomics for gene cluster identification.
Main Methods:
- Literature review focusing on accessory chromosomes and secondary metabolism.
- Analysis of studies integrating untargeted metabolomics and genome sequencing.
- Examination of biosynthetic gene clusters for secondary metabolites, including mycotoxins.
Main Results:
- Accessory chromosomes are crucial for virulence and secondary metabolite production in pathogenic fungi.
- Horizontal transfer and core chromosome interactions contribute to accessory chromosome evolution.
- Untargeted metabolomics and genome sequencing effectively link secondary metabolites to their accessory chromosome-located biosynthetic gene clusters.
- Studies in *Alternaria* and *Fusarium* reveal insights into toxin biosynthesis and enzyme evolution.
Conclusions:
- Accessory chromosomes are key drivers of fungal pathogenicity and secondary metabolite diversity.
- Understanding accessory chromosome evolution is vital for managing fungal diseases.
- Integrated omics approaches are powerful tools for discovering fungal secondary metabolite pathways.
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