SummaryWhile much is known about the biosynthesis of secondary metabolites by filamentous fungi their biological role is often less clear. The assumption is these pathways have adaptive value to the organism but often the evidence to support this role is lacking. We provide the first genetic evidence that the fungal produced secondary metabolite, peramine, protects a host plant from insect herbivory. Peramine is a potent insect feeding deterrent synthesized by Epichloë/ Neotyphodium mutualistic endophytes in association with their grass hosts. The structure of peramine, a pyrrolopyrazine, suggests that it is the product of a reaction catalysed by a two-module non-ribosomal peptide synthetase (NRPS). Candidate sequences for a peramine synthetase were amplified by reverse transcription polymerase chain reaction. Four unique NRPS products were identified, two of which were preferentially expressed in planta . One of these hybridized to known peramine producing strains. This clone was used to isolate an Epichloë festucae cosmid that contained a two-module NRPS, designated perA . Nine additional genes, which show striking conservation of microsynteny with Fusarium graminearum and other fungal genomes, were identified on the perA -containing cosmid. Associations between perennial ryegrass and an E. festucae mutant deleted for perA lack detectable levels of peramine. A wild-type copy of perA complemented the deletion mutant, confirming that perA is a NRPS required for peramine biosynthesis. In a choice bioassay, plant material containing the perA mutant was as susceptible to Argentine stem weevil (ASW) ( Listronotus bonariensis ) feeding damage as endophyte-free plants confirming that peramine is the E. festucae metabolite responsible for ASW feeding deterrent activity.

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Two exotic pests, Argentine stem weevil (ASW) and clover root weevil (CRW) are causing damage estimated at up to $200 M p.a. and $235 M p.a. respectively in dairy and sheep and beef pastures. While CRW is subject to successful biological control management it still causes considerable losses. Lesser pests also contribute to lost production, particularly as they often coexist with more major pests. However, their economic cost to New Zealand is difficult to calculate due to the variable nature of infestations on both temporal and spatial scales. At farm and paddock level, it is abundantly clear that substantial savings could be made if pest management is achieved. It is equally clear that in many instances the tools to do so are limited but if developed would contribute substantially to farm profitability.

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Ryegrass staggers is a seasonal mycotoxicosis of grazing livestock characterised by tremors, in coordination and a staggering gait almost unaccompanied by physical lesions. Deaths occur only as a consequence of accident or starvation. Outbreaks, in summer and autumn, occur only on pasture in which endophyte (Neotyphodium lolii)-infected perennial ryegrass (Lolium perenne) predominates and usually on which animals are grazed intensively. Animals recover when moved to a different type of grazing or after rain has promoted pasture growth. The disease was recognised for 80 years before its cause was discovered as a consequence of a grazing trial of sheep on three ryegrass cultivars which happened to have three different levels of endophyte infection. The endophyte was first formally described as Acremonium loliae, later corrected to Acremonium lolii, and was finally placed in the genus Neotyphodium. It produces a number of secondary metabolites of which lolitrem B is the principal one causing ryegrass staggers symptoms. Ergopeptides are also produced which cause heat stress and lack of productivity. N. lolii is symptomless in the plant, seed borne and grows intercellularly in the aerial parts, mainly in reproductive tillers and leaf sheaths but sparsely in leaf blades. It dies in stored seed and infection rates of different ryegrass cultivars have depended on seed storage times during their production. In addition, N. Lolii produces insect feeding deterrents, among them peramine, which protects infected plants from pest predation. Because of this, control of ryegrass staggers by elimination of endophyte-infected ryegrass is not feasible in areas in which insect predation is a serious pasture problem. However, N. lolii strains vary in the secondary metabolites they produce allowing the selection of strains that produce desirable metabolites. By inoculating such strains into uninfected ryegrass plants it is possible to produce cultivars which do not cause ryegrass staggers but resist insect predation. This review aims to provide a comprehensive summary of the current understanding of the N. lolii / L. perenne symbiosis, the toxins it is known to produce, their effects on animals and plants and the strategies used to control their ill effects while maximising their beneficial ones.