Transcriptomics reveals the mycoparasitic strategy of the mushroom Entoloma abortivum on species of the mushroom Armillaria

During mycoparasitism, a fungus—the host—is parasitized by another fungus—the mycoparasite. The genetic underpinnings of these relationships have been best characterized in Ascomycete fungi. However, within Basidiomycete fungi, there are rare instances of mushroom-forming species parasitizing the reproductive structures, or sporocarps, of other mushroom-forming species. One of the most enigmatic of these occurs between Entoloma abortivum and species of Armillaria, where hyphae of E. abortivum are hypothesized to disrupt the development of Armillaria sporocarps, resulting in the formation of carpophoroids. However, it remains unknown whether carpophoroids are the direct result of a mycoparasitic relationship. To address the nature of this unique interaction, we analyzed gene expression of field-collected Armillaria and E. abortivum sporocarps and carpophoroids. Transcripts in the carpophoroids are primarily from E. abortivum, supporting the hypothesis that this species is parasitizing Armillaria. Most notably, we identified differentially expressed E. abortivum β-trefoil-type lectins in the carpophoroid, which we hypothesize bind to Armillaria cell wall galactomannoproteins, thereby mediating recognition between the mycoparasite and the host. The most significantly upregulated E. abortivum transcripts in the carpophoroid code for oxalate decarboxylases—enzymes that degrade oxalic acid. Oxalic acid is a virulence factor in many plant pathogens, including Armillaria species, however, E. abortivum has evolved a sophisticated strategy to overcome this defense mechanism. The number of gene models and genes that code for carbohydrate-active enzymes in the E. abortivum transcriptome were reduced compared to other closely related species, perhaps as a result of the specialized nature of this interaction. Field-collected sporocarps (fruiting bodies) for each species in this interaction--Entoloma abortivum and Armillaria mellea--were sequenced. For each species, three biological replicates of individual sporocarps were sequenced and three technical replicates of each of those biological replicates were also sequenced. Sporocarps were considered "baseline" treatments. Then for the mixed tissue, or carpophoroids, which contain both E. abortivum and A. mellea, three biological replicates were also sequenced, along with three technical replicates for each biological replicate. Gene expression for each species was analyzed as to how it differed between the sporocarps and carpophoroids.