Specialized plant biochemistry drives gene clustering in fungi

Abstract

The fitness and evolution of both prokaryotes and eukaryotes are affected by the organization of their genomes. In particular, the physical clustering of functionally related genes can facilitate coordinated gene expression and can prevent the breakup of co-adapted alleles in recombining populations. While clustering may thus result from selection for phenotype optimization and persistence, the extent to which eukaryotic gene organization in particular is driven by specific environmental selection pressures has rarely been systematically explored. Here, we investigated the genetic architecture 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 over one thousand gene clusters, as well as many conserved combinations of clusters, in a phylogenetically and ecologically diverse set of fungal genomes. We demonstrate that congruence in gene organization over small spatial scales in fungal genomes 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 in 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 gene organization and ecological evolution in this ancient eukaryotic lineage.