Abstract
Ramularia collo-cygni causes Ramularia leaf spot (RLS) disease of barley. The fungus develops asymptomatically within its host until late in the growing season, when necrotic lesions become visible on upper leaves. Fungal secondary metabolites (SM) have been proposed as important factors in RLS lesion formation but the biosynthetic pathways involved remain largely unknown. Mining the R. collo-cygni genome revealed the presence of 10 polyketide synthases (PKS), 10 nonribosomal peptide synthetases (NRPS), and 3 hybrid PKS-NRPS (HPS) identified within clusters of genes with predicted functions associated with secondary metabolism. SM core genes along with their predicted transcriptional regulators exhibited transcriptional coexpression during infection of barley plants. Moreover, their expression peaked during early stages of host colonization and preceded or overlapped with the appearance of disease symptoms, suggesting that SM may manipulate the host to promote colonization or protect R. collo-cygni from competing organisms. Accordingly, R. collo-cygni inhibited the growth of several fungi in vitro, indicating that it synthesized and excreted antifungal agents. Taken together, these findings demonstrate that the R. collo-cygni genome contains the genetic architecture to synthesize a wide range of SM and suggests that coexpression of PKS and HPS is associated with competitive colonization of the host and early symptom development.
Highlights
Ramularia leaf spot (RLS) is a late-season disease of barley (Hordeum vulgare) occurring in temperate regions worldwide
Using Basic Local Alignment Search Tool (BLAST) combined with domain analysis, the R. collo-cygni genome was found to contain 21 genes encoding for proteins containing domains associated with polyketide synthases (PKS) and 25 genes encoding proteins exhibiting a domain associated with nonribosomal peptide synthetases (NRPS)
The R. collo-cygni genome contains at least 23 potentially functional secondary metabolites (SM) core genes belonging to the PKS, NRPS, and hybrid PKS-NRPS (HPS) families
Summary
Identification of secondary metabolism-related core genes in R. collo-cygni. Using Basic Local Alignment Search Tool (BLAST) combined with domain analysis, the R. collo-cygni genome was found to contain 21 genes encoding for proteins containing domains associated with PKS and 25 genes encoding proteins exhibiting a domain associated with NRPS. Eight of the identified PKS and all three HPS core genes appeared to be located in a cluster containing several genes with a predicted function associated with secondary metabolism (Fig. 2). Two putative SM clusters surrounding a PKS core gene (Pks and Pks, identified on scaffold m24 and contig 58, respectively) and two located near a HPS gene (Hps and Hps, identified on contig 1 and contig 14, respectively) contained predicted transcription factors with GAL4 domains, known as Zn(II)2Cys DNA-binding domains, that have been shown to regulate secondary metabolism in fungal pathogens (Brakhage 2013). Three of the SM-related gene clusters found in R. collo-cygni exhibited high similarity to clusters involved in the biosynthesis of SM previously characterized in another fungal species (Fig. 3; Supplementary Table S4). The relationship between R. collo-cygni core genes and core genes in other fungal species was further examined by a
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