Abstract

The ecological importance of the duplication and diversification of gene clusters that synthesize secondary metabolites in fungi remains poorly understood. Here, we demonstrated that the duplication and subsequent diversification of a gene cluster produced two polyketide synthase gene clusters in the cosmopolitan fungal genus Metarhizium. Diversification occurred in the promoter regions and the exon-intron structures of the two Pks paralogs (Pks1 and Pks2). These two Pks genes have distinct expression patterns, with Pks1 highly expressed during conidiation and Pks2 highly expressed during infection. Different upstream signaling pathways were found to regulate the two Pks genes. Pks1 is positively regulated by Hog1-MAPK, Slt2-MAPK and Mr-OPY2, while Pks2 is positively regulated by Fus3-MAPK and negatively regulated by Mr-OPY2. Pks1 and Pks2 have been subjected to positive selection and synthesize different secondary metabolites. PKS1 is involved in synthesis of an anthraquinone derivative, and contributes to conidial pigmentation, which plays an important role in fungal tolerance to UV radiation and extreme temperatures. Disruption of the Pks2 gene delayed formation of infectious structures and increased the time taken to kill insects, indicating that Pks2 contributes to pathogenesis. Thus, the duplication of a Pks gene cluster and its subsequent functional diversification has increased the adaptive flexibility of Metarhizium species.

Highlights

  • Metabolic gene clusters are hotspots for the generation of fungal metabolic diversity through gene duplication, but the ecological importance of these gene clusters remains poorly understood [1]

  • We found that PKS1 is involved in synthesis of an anthraquinone derivative

  • Two polyketide synthase (Pks) gene clusters in Metarhizium species result from a gene cluster duplication Using the PKS1 (MAA_07745) and PKS2 (MAA_03239) protein sequences in M. robertsii as queries, we performed a reciprocal BLASTP against the NCBI Fungal database

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Summary

Introduction

Metabolic gene clusters are hotspots for the generation of fungal metabolic diversity through gene duplication, but the ecological importance of these gene clusters remains poorly understood [1]. Type I polyketides are common in fungi; they are usually synthesized by gene clusters that include polyketide synthase (Pks) genes [2, 3]. Fungi often have multiple Pks gene clusters as a result of gene duplication (typically) and horizontal gene transfer (less often) [1, 4,5,6]. Further diversification of Pks gene clusters might occur via lineage-specific duplication and loss events, or via functional divergences in response to ecological pressures [3, 4]. Functional analyses have shown that the SMs synthesized by some Pks gene clusters have important biological functions. Little is known about the relationship between the evolutionary diversification of Pks gene clusters and ecological adaptation in fungi

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