A novel family of cyclic oligopeptides derived from ribosomal peptide synthesis of an in planta-induced gene, gigA, in Epichloë endophytes of grasses

• Published in: Fungal genetics and biology 2015-12, Vol.85, p.14-24
• Main Authors: Johnson, Richard D., Lane, Geoffrey A., Koulman, Albert, Cao, Mingshu, Fraser, Karl, Fleetwood, Damien J., Voisey, Christine R., Dyer, Jolon M., Pratt, Jennifer, Christensen, Michael, Simpson, Wayne R., Bryan, Gregory T., Johnson, Linda J.
• Format: Article
• Language: English
• Subjects: Cyclic oligopeptide; Endophytes - genetics; Endophytes - physiology; Epichloe - genetics; Epichloe - physiology; Epichloë; Epichloëcyclin; Fungal Proteins - chemistry; Fungal Proteins - genetics; Fungal Proteins - metabolism; Oligopeptides - genetics; Oligopeptides - metabolism; Peptides, Cyclic - genetics; Peptides, Cyclic - metabolism; Poaceae - microbiology; Protein Biosynthesis; Ribosomal peptide synthetic pathway; Ribosomal Proteins - chemistry; Ribosomal Proteins - metabolism; Symbiosis; Tandem Mass Spectrometry
• ISSN: 1087-1845; 1096-0937
• DOI: 10.1016/j.fgb.2015.10.005

•A group of cyclic peptides (epichloëcyclins) are the product of a single gene, gigA.•gigA encodes a small secreted protein containing an imperfect 27 amino acid repeat.•Epichloëcyclins vary due to both sequence and repeat number within the gigA gene.•Epichloëcyclins are synthesised by a ribosomal peptide synthetic (RiPS) pathway. Fungal endophytes belonging to the genus Epichloë form associations with temperate grasses belonging to the sub-family Poöideae that range from mutualistic through to pathogenic. We previously identified a novel endophyte gene (designated gigA for grass induced gene) that is one of the most abundantly expressed fungal transcripts in endophyte-infected grasses and which is distributed and highly expressed in a wide range of Epichloë grass associations. Molecular and biochemical analyses indicate that gigA encodes a small secreted protein containing an imperfect 27 amino acid repeat that includes a kexin protease cleavage site. Kexin processing of GigA liberates within the plant multiple related products, named here as epichloëcyclins, which we have demonstrated by MS/MS to be cyclic peptidic in nature. Gene deletion of gigA leads to the elimination of all epichloëcyclins with no conspicuous phenotypic impact on the host grass, suggesting a possible bioactive role. This is a further example of a ribosomal peptide synthetic (RiPS) pathway operating within the Ascomycetes, and is the first description of such a pathway from a mutualistic symbiotic fungus from this Phylum.