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Endophytic Epichloë (Clavicipitaceae) association with Lolium perenne and Lolium arundinaceum (Poaceae) resulting in health problems for the livestock and horses in temperate Australian pastures: assay of secondary metabolites and antioxidant activity

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Abstract

Livestock grazing in pastures that include large populations of Lolium perenne and Lolium arundinaceum were found to be suffering a ‘curious’ neurological problem in the late 1950s, which was subsequently named as the ‘ryegrass staggers’, because the sheep suffered that problem when they fed on the perennial ryegrass, L. perenne. The chemicals that trigger staggers in the livestock have been resolved: tremorgenic alkaloids, especially lolitrems of the indole-diterpene group, particularly lolitrem B, that are synthesized during the biotrophic association of Epichloë festucae var. lolii in the shoots of L. perenne and L. arundinaceum. With an agenda posted to us in Charles Sturt University, Orange Campus, New South Wales, we investigated the quality and quantity of secondary metabolites and assayed the antioxidant capacity of the phenolics using populations of L. perenne and L. arundinaceum that included determined strains of E. festucae var. lolii and E. coenophiala obtained from different localities of temperate Australia. N-acetylnorloline was detected only in E. coenophiala (strain AR542) infected L. arundinaceum, regardless of being of either the Mediterranean or the Continental cultivars. Tridecanoic, n-capric, eicosatrienoic, and linoleic acids were detected in all the tested L. arundinaceum cultivars, irrespective of either their cultivar or their endophyte status. Phenolic extracts from L. perenne infected with Epichloë ‘wild type’ scavenged DPPH (2, 2-diphenyl-1-picrylhydrazyl) at a much faster rate than that infected with AR1, AR37, and that free of Epichloë. The extracts from the Epichloë-free Mediterranean L. arundinaceum showed the maximum antioxidant capacity, followed by the Epichloë-free Continental L. arundinaceum. Lolium perenne infected with Epichloë ‘wild-type’ showed the greatest scavenging capacity, whereas the endophyte-free L. perenne showed the least. Those L. perenne populations infected with strains AR1 and AR37 showed intermediate capacities. Alkaloids synthesized in Epichloë-infected Poaceae induce toxicity in horses, cattle, and sheep. Today we know of most of the secondary metabolites produced in Epichloë-infected Poaceae. Ergot alkaloids (e.g., ergoamides) induce psychotropic effects in consumer animals, whereas vasomotor effects are less pronounced. Ergopeptides and their derivatives usually occur in Epichloë-infected Lolium-s, especially in L. arundinaceum. Ergopeptines cause vasomotor effects resulting in ‘fescue foot’, which is, invariably, aggravated by elevated atmospheric temperature. Ergovaline, another abundant Epichloë-derived alkaloid in poaceous seeds, presently known to bear the greatest vasomotor effect. Studies made, thus far, clarify that interactions with drug-metabolizing enzymes happen and these interactions have a role in the elevating the toxicity levels of the ergot-family of alkaloids.

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Fig. 1
Fig. 2
Fig. 3

Source: https://en.wikipedia.org/wiki/Ergovaline#/media/File:Ergovaline.svg, public domain

Fig. 4

Source: Qawasmeh et al. 2011

Fig. 5

Source: Qawasmeh et al. 2011

Fig. 6

Source: Qawasmeh et al. 2012a

Fig. 7

Source: Qawasmeh et al. 2012a

Fig. 8

Source: Qawasmeh et al. 2012b

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Acknowledgements

Thanks are due to Anamika Sharma (Montana State University, Conrad, USA) for help with the arrangement of figures and tables.

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    Anantanarayanan Raman

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Raman, A. Endophytic Epichloë (Clavicipitaceae) association with Lolium perenne and Lolium arundinaceum (Poaceae) resulting in health problems for the livestock and horses in temperate Australian pastures: assay of secondary metabolites and antioxidant activity. Plant Physiol. Rep. 24, 474–486 (2019). https://doi.org/10.1007/s40502-019-00481-9

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