Specialized plant biochemistry drives gene clustering in fungi

The fitness and evolution of prokaryotes and eukaryotes are affected by the organization of their genomes. In particular, the physical clustering of genes can coordinate gene expression and can prevent the breakup of co-adapted alleles. Although clustering may thus result from selection for phenotype optimization and persistence, the impact of environmental selection pressures on eukaryotic genome organization has rarely been systematically explored. Here, we investigated the organization of fungal genes involved in the degradation of phenylpropanoids, a class of plant-produced secondary metabolites that mediate many ecological interactions between plants and fungi. Using a novel gene cluster detection method, we identified 1110 gene clusters and many conserved combinations of clusters in a diverse set of fungi. We demonstrate that congruence in genome organization over small spatial scales is often associated with similarities in ecological lifestyle. Additionally, we find that while clusters are often structured as independent modules with little overlap in content, certain gene families merge multiple modules into a common network, suggesting they are important components of phenylpropanoid degradation strategies. Together, our results suggest that phenylpropanoids have repeatedly selected for gene clustering in fungi, and highlight the interplay between genome organization and ecological evolution in this ancient eukaryotic lineage.

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