A review of theNeotyphodium lolii / Lolium perennesymbiosis and its associated effects on animal and plant health, with particular emphasis on ryegrass staggers

Abstract

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.

The occurrence of ryegrass staggers and heat stress in sheep grazing ryegrass-endophyte associations with diverse alkaloid profiles

“…The threshold concentration of lolitrem B required to induce ryegrass staggers is accepted to be 1.8-2.5 mg/kg in herbage (di Menna et al 2012). In 2013, concentrations of lolitrem B concentrations exceeded this threshold in S-STD pastures (4.1 mg/kg) and severe staggers was observed.…”

“…Peramine is known to have potent activity against Argentine stem weevil (Listronotus bonariensis) which is a major pest of pastures, but it has no adverse effects on livestock (Rowan 1993;Pownall et al 1995). In contrast, lolitrem B is the cause of ryegrass staggers and has some minor effects on Argentine stem weevil (Fletcher and Harvey 1981;Fletcher 1982;di Menna et al 2012). Ergovaline causes heat stress (Klotz 2015), as well as giving ryegrass protection against black beetle (Heteronychus arator) (Ball et al 1997;Popay and Hume 2011).…”

Plant Bioactive Metabolites and Drugs Produced by Endophytic Fungi of Spermatophyta

“…We also do not consider the complex case of the endophytic fungi inhabiting a series of fodder plants, which cause noxious effects to livestock because of their attitude to permeate host tissues with mycotoxins, and are also able to produce phytohormones [8][9][10]. A few excellent reviews on this bordering subject are available in the literature [11][12][13].…”

Elimination of the tremorgenic toxin of Ipomoea asarifolia by milk

“…The cause of death of the pups from Group 3, that ingest the highest amount of plant (30% in the food), was not determined, but the fact that all offspring of each dam died in the same day suggest that the death was due to the toxin present in the milk. The tremorgenic compounds toxic to livestock include indole-diterpenes comprising the penitrem A, B and C produced in Lolium perenne by the endophyte Neothyphodium lolii (Di Menna et al 2012) and by various species of Penicillium (Botha et al 1996), paxilline produced also by Neothyphodium lolii (di Menna et al 2012), and paspalitrem and paspaline produced by Claviceps spp. (Cawdell-Smith et al 2010).…”

“…I. asarifolia is a tremorgenic plant that causes poisoning in sheep (Döbereiner et al 1960, Guedes et al 2007), goats (Döbereiner et al 1960, Medeiros et al 2003, Guedes et al 2007), cattle (Döbereiner et al 1960, Barbosa et al 2005) and buffalo (Barbosa et al 2005). Clinical signs caused by I. asarifolia are similar than those caused by the indole-diterpene mycotoxins produced by different fungi (di Menna et al 2012, Cawdell-Smith et al 2010, but the tremorgenic toxin of the plant is unknown.In With the aim to determine if the tremorgenic toxin of Ipomoea asarifolia is eliminated in milk, three groups of Swiss female mice received, immediately after giving birth until weaning, a ration containing 20% or 30% of dry I. asarifolia. All the offspring of the females that received 20% or 30% I. asarifolia showed tremors 2-4 days after birth.…”