Abstract
BackgroundFungal plant pathogens pose major threats to crop yield and sustainable food production if they are highly adapted to their host and the local environment. Variation in gene expression contributes to phenotypic diversity within fungal species and affects adaptation. However, very few cases of adaptive regulatory changes have been reported in fungi and the underlying mechanisms remain largely unexplored. Fungal pathogen genomes are highly plastic and harbor numerous insertions of transposable elements, which can potentially contribute to gene expression regulation. In this work, we elucidated how transposable elements contribute to variation in melanin accumulation, a quantitative trait in fungi that affects survival under stressful conditions.ResultsWe demonstrated that differential transcriptional regulation of the gene encoding the transcription factor Zmr1, which controls expression of the genes in the melanin biosynthetic gene cluster, is responsible for variation in melanin accumulation in the fungal plant pathogen Zymoseptoria tritici. We show that differences in melanin levels between two strains of Z. tritici are due to two levels of transcriptional regulation: (1) variation in the promoter sequence of Zmr1 and (2) an insertion of transposable elements upstream of the Zmr1 promoter. Remarkably, independent insertions of transposable elements upstream of Zmr1 occurred in 9% of Z. tritici strains from around the world and negatively regulated Zmr1 expression, contributing to variation in melanin accumulation.ConclusionsOur studies identified two levels of transcriptional control that regulate the synthesis of melanin. We propose that these regulatory mechanisms evolved to balance the fitness costs associated with melanin production against its positive contribution to survival in stressful environments.
Highlights
Fungal plant pathogens pose major threats to crop yield and sustainable food production if they are highly adapted to their host and the local environment
Differences in melanin accumulation are determined by the polyketide synthase 1 (Pks1) cluster Melanin accumulation in the Swiss Z. tritici strain 3D1 was lower than that in the strain 3D7 at early time points (10 days post inoculation, dpi)
We demonstrated that diversity in melanin accumulation is determined by differential regulation of gene expression instead of through mutations in coding sequences
Summary
Fungal plant pathogens pose major threats to crop yield and sustainable food production if they are highly adapted to their host and the local environment. Variation in gene expression contributes to phenotypic diversity within fungal species and affects adaptation. Fungal pathogen genomes are highly plastic and harbor numerous insertions of transposable elements, which can potentially contribute to gene expression regulation. Most of the adaptive mutations identified until now are in coding sequences [4,5,6] The reason for this is that protein variants are easier to identify because the Mutations outside of coding regions can lead to alterations in transcription, splicing, transcript stability, or chromatin remodeling and can affect the regulation of gene expression [6,7,8]. Transposable element insertions have the potential to contribute to phenotypic diversity through chromatin remodeling and regulation of gene expression
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