Endophyte metabolites associated with perennial ryegrass toxicosis
K. F. M. Reed A E , W. J. Mace B , L. V. Walker C and L. R. Fletcher DA Reed Pasture Science, Brighton East, Vic. 3187, Australia.
B AgResearch Limited, Grasslands Research Centre, Private Bag 11008, Palmerston North 4442, New Zealand.
C Southern Scientific Services, PO Box 234, Hamilton, Vic. 3300, Australia.
D AgResearch Limited, Lincoln Research Centre, Private Bag 4749, Christchurch 8140, New Zealand.
E Corresponding author. Email: rps@eftel.net
Animal Production Science 56(5) 895-907 https://doi.org/10.1071/AN14495
Submitted: 21 February 2014 Accepted: 12 October 2014 Published: 20 February 2015
Abstract
Perennial ryegrass (PRG) was analysed for alkaloids associated with the expression of perennial ryegrass endophyte toxicosis (PRGT) in south-east Australia. Over two seasons, the PRG cultivar Samson (‘high endophyte’, viz. naturally infected with a wild-type strain of Epichloë festucae var. lolii) was sampled on five occasions during November to May at four farms in Victoria and at Lincoln, New Zealand. Endophyte frequency in the populations was 77–100%. PRG was also sampled from 20 Victorian and Tasmanian farm pastures where stock were experiencing PRGT (endophyte infection frequencies of 87–100%). The Victorian summer of 2010–11 was atypically moist; pasture remained green. Lolitrem B was consistently high at Lincoln and 2–3 times that observed in Victorian samples of isogenetic PRG, or in PRG causing PRGT; it was the dominant toxin in 2011 with concentrations commonly exceeding the tolerance level of 1.8 mg/kg. In the following year, one with a more typical summer, ergovaline was the dominant toxin. Liquid Chromatography–Mass Spectrometry/Mass Spectrometry (LC-MS/MS) was carried out to determine indole diterpene intermediates in the lolitrem B biosynthesis pathway and for ergot alkaloid intermediates in the ergovaline pathway. The values for lolitrem B determined by LC-MS/MS correlated strongly with those obtained using high pressure liquid chromatography. In both Years 1 and 2, significantly higher expression was observed in the Lincoln relative to Victorian samples of PRG for paspaline, terpendole C, lolitrem E, lolitrem B and lolitrem F. For the ergot alkaloids, significant differences were not apparent between Victorian and Lincoln samples in Year 1. In Year 2, LC-MS/MS results showed ergovaline concentrations were greater in Victorian samples. In addition to endophyte-produced toxins, ergot alkaloids produced by Claviceps purpurea (ergotamine, ergocryptine and ergocornine) were detected in grass samples on 6/27 occasions. Some unidentified metabolites were noted in both Victorian and Lincoln samples. The effects of ingested vaso-constrictive ergot alkaloids combined with that of high solar radiation on ruminants’ heat load are considered most important with respect to the occasionally severe expression of PRGT in Australia.
Additional keywords: Claviceps purpurea, Epichloë festucae var. lolii, ergot alkaloids, ergovaline, heat stress, indole diterpenes, lolitrem, perennial ryegrass toxicoses.
References
Blaney BJ, McKenzie RA, Walters JA, Taylor LF, Bewg WS, Ryley MJ, Maryam R (2000) Sorghum ergot (Claviceps africana) associated with agalactica and feed refusal in pigs and dairy cattle. Australian Veterinary Journal 78, 102–107.| Sorghum ergot (Claviceps africana) associated with agalactica and feed refusal in pigs and dairy cattle.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3c3gtV2juw%3D%3D&md5=4249bd2a6bb18276c62974d25d248917CAS | 10736670PubMed |
Bluett SJ, Thom ER, Clark DA, Macdonald KA, Minneé EMK (2005) Effects of perennial ryegrass infected with either AR1 or wild endophyte on dairy production in the Waikato. New Zealand Journal of Agricultural Research 48, 197–212.
| Effects of perennial ryegrass infected with either AR1 or wild endophyte on dairy production in the Waikato.Crossref | GoogleScholarGoogle Scholar |
Burke JM, Speirs DE, Kojima FN, Perry GA, Salfen BE, Wood SL, Patterson DJ, Smith MF, Lucy MC, Jackson WG, Piper EL (2001) Interaction of endophyte-infected fescue and heat stress on ovarian function in the beef heifer. Biology of Reproduction 65, 260–268.
| Interaction of endophyte-infected fescue and heat stress on ovarian function in the beef heifer.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXkslWhur0%3D&md5=4bf4b38e6759bd032209d493c20b4aedCAS | 11420248PubMed |
Combs MDA, Rendell D, Reed KFM, Mace WJ, Quinn JC (2014) Dehydration and electrolyte disturbances contribute to severity of symptoms associated with perennial ryegrass toxicosis in Australia – insights from the 2011 outbreak. Australian Veterinary Journal 92, 107–113.
Gallagher RT, Hawkes AD, Steyn PS, Vleggaar R (1984) Tremorgenic neurotoxins from perennial ryegrass causing ryegrass staggers disorder of livestock: structure elucidation of lolitrem B. Journal of the Chemical Society. Chemical Communications 614–616.
| Tremorgenic neurotoxins from perennial ryegrass causing ryegrass staggers disorder of livestock: structure elucidation of lolitrem B.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2cXmtlSrsrc%3D&md5=4a5e74dd461cd3d00e7b175441bd1eddCAS |
Genstat Committee (2008) ‘Genstat for Windows.’ 11th edn. (VSN International: Hertfordshire, UK)
Hiatt EE, Hill NS, Bouton JH, Stuedemann JA (1999) Tall fescue endophyte detection: commercial immunoblot test kit compared with microscopic analysis. Crop Science 39, 796–799.
| Tall fescue endophyte detection: commercial immunoblot test kit compared with microscopic analysis.Crossref | GoogleScholarGoogle Scholar |
Lane GA (1999) Chemistry of endophytes: pattern and diversity. In ‘Ryegrass endophyte: an essential New Zealand symbiosis’. New Zealand Grassland Association, Grassland Research and Practice Series No.7. (Eds DR Woodfield, C Matthew) pp. 85–94. (New Zealand Grassland Association: Palmerston North, New Zealand)
Lane GA, Tapper BA, Davies E (1999) Ergot alkaloids additional to ergovaline in endophyte-infected perennial ryegrass and tall fescue in New Zealand. In ‘Ryegrass endophyte: an essential New Zealand symbiosis’. New Zealand Grassland Association, Grassland Research and Practice Series No.7. (Eds DR Woodfield, C Matthew) pp. 95–100. (New Zealand Grassland Association: Palmerston North, New Zealand)
Moore KJ, Moser LE, Vogel KP, Waller SS, Johnson BE, Pedersen JF (1991) Describing and quantifying growth stages of perennial forage grasses. Agronomy Journal 83, 1073–1077.
| Describing and quantifying growth stages of perennial forage grasses.Crossref | GoogleScholarGoogle Scholar |
Panaccione D (2005) Origins and significance of ergot alkaloid diversity in fungi. FEMS Microbiology Letters 251, 9–17.
| Origins and significance of ergot alkaloid diversity in fungi.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtVWgsr%2FN&md5=8f17936130818660013bdd773bc5553bCAS | 16112823PubMed |
Rasmussen S, Lane GA, Mace W, Parsons AJ, Fraser K, Xue H (2012) The use of genomics and metabolomics methods to quantify fungal endosymbionts and alkaloids in grasses. In ‘Plant metabolomics: methods and protocols, methods in molecular biology, Vol. 860’. (Eds NW Hardy, RD Hall) pp. 213–226. (Springer: New York, NY)
Reed KFM, Moore DD (2009) A preliminary survey of zearalenone and other mycotoxins in Australian silage and pasture. Animal Production Science 49, 696–703.
| A preliminary survey of zearalenone and other mycotoxins in Australian silage and pasture.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXovFOqsL0%3D&md5=cd85ba310a06338279ae904e279bd625CAS |
Reed KFM, Walsh JR, Cross PA, McFarlane NM, Sprague M (2004) Ryegrass endophyte (Neotyphodium lolii) alkaloids and mineral concentrations in perennial ryegrass (Lolium perenne) from southwest Victorian pasture. Australian Journal of Experimental Agriculture 44, 1185–1194.
| Ryegrass endophyte (Neotyphodium lolii) alkaloids and mineral concentrations in perennial ryegrass (Lolium perenne) from southwest Victorian pasture.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXmsVOnsw%3D%3D&md5=5f12adf950c75fa46e4fa6f2c53d3fadCAS |
Reed KFM, Webb Ware J (2012) Management of perennial ryegrass endophyte toxicoses. Publication code: 9781741919509. (Meat and Livestock Australia: Sydney) Available at http://www.mla.com.au/News-and-resources/Publication-details?pubid=5997 [Verified 28 June 2014]
Reed KFM, Scrivener CJ, Rainsford KA, Walker LV (2005) Neotyphodium research and application in Australia. In ‘Neotyphodium in cool season grasses’. (Eds CA Roberts, CP West, DE Spiers) pp. 43–54. (Blackwell: Ames, IA)
Reed KFM, Nie ZN, Walker LV, Mace WJ, Clark SG (2011b) Pasture and weather characteristics associated with outbreaks of perennial ryegrass toxicosis in southern Australia. Animal Production Science 51, 738–752.
| Pasture and weather characteristics associated with outbreaks of perennial ryegrass toxicosis in southern Australia.Crossref | GoogleScholarGoogle Scholar |
Reed KFM, Nie ZN, Walker LV, Kearney G (2011c) Fluctuations in the concentration of ergovaline and lolitrem B produced by the wild-type endophyte (Neotyphodium lolii) in perennial ryegrass pasture. Animal Production Science 51, 1098–1108.
| Fluctuations in the concentration of ergovaline and lolitrem B produced by the wild-type endophyte (Neotyphodium lolii) in perennial ryegrass pasture.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhsFertb3L&md5=ffe16c5df7343f5f34ef8af0f587bffdCAS |
Sackett D, Francis J (2006) The economic assessment of the impact of wild endophyte-infected perennial ryegrass (Lolium perenne) on the productivity of sheep and cattle and the profitability of Australian livestock enterprises. Report AHW.089, Meat and Livestock Australia, North Sydney.
Sackett D, Holmes P, Abbott K, Jephcott S, Barber M (2006) Assessing the economic cost of endemic disease on the profitability of Australian beef cattle and sheep producers. Report AHW.087. Meat and Livestock Australia, North Sydney.
Saikia S, Nicholson MJ, Young C, Parker EJ, Scott B (2008) The genetic basis for indole-diterpene chemical diversity in filamentous fungi. Mycological Research 112, 184–199.
| The genetic basis for indole-diterpene chemical diversity in filamentous fungi.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXlsFOhsLg%3D&md5=c9fa7334b32f8a9394e369ebf74f456fCAS | 18262778PubMed |
Shelby R, Flieger M (1997) Improved method of analysis for ergovaline in Tall Fescue by High Performance Liquid Chromatography. Journal of Agricultural and Food Chemistry 45, 1797–1800.
| Improved method of analysis for ergovaline in Tall Fescue by High Performance Liquid Chromatography.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXjtlWrtr8%3D&md5=d3cd68e4747023d5eae6d6ad33efe2e0CAS |
Shelby RA, Olsovska J, Havlicek V, Flieger M (1997) Analysis of ergot alkaloids in endophyte-infected tall fescue by liquid chromatography/electrospray ionization mass spectroscopy. Journal of Agricultural and Food Chemistry 45, 4674–4679.
| Analysis of ergot alkaloids in endophyte-infected tall fescue by liquid chromatography/electrospray ionization mass spectroscopy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXnsVSks7w%3D&md5=50b85d4b47cb3a068482d99d46fcbe94CAS |
Spiering MJ, Davies E, Tapper BA, Schmid J, Lane GA (2002) Simplified extraction of ergovaline and peramine for analysis of tissue distribution in endophyte-infected grass tillers. Journal of Agricultural and Food Chemistry 50, 5856–5862.
| Simplified extraction of ergovaline and peramine for analysis of tissue distribution in endophyte-infected grass tillers.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XmvFKrsLg%3D&md5=1ddbb6dba32371a17784b4c4f1e78bd6CAS | 12358450PubMed |
Spiering MJ, Lane GA, Christensen MJ, Schmid J (2005) Distribution of the fungal endophyte Neotyphodium lolii is not a major determinant of the distribution of fungal alkaloids in Lolium perenne plants. Phytochemistry 66, 195–202.
| Distribution of the fungal endophyte Neotyphodium lolii is not a major determinant of the distribution of fungal alkaloids in Lolium perenne plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXksVektw%3D%3D&md5=cd0fac7a48157177199f809bb79ec843CAS | 15652576PubMed |
Strickland JR, Looper ML, Matthews JC, Rosenkrans CF, Flythe MD, Brown KR (2011) Board-invited review: St Anthony’s fire in livestock: causes, mechanisms and potential solutions. Journal of Animal Science 89, 1603–1626.
| Board-invited review: St Anthony’s fire in livestock: causes, mechanisms and potential solutions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXls1Ohsrk%3D&md5=302a64036b7e9c7490d1568b3ac7609aCAS | 21521821PubMed |
Thom ER, Waugh CD, Minneé EMK, Waghorn GC (2013) Effects of novel and wild-type endophytes in perennial ryegrass on cow health and production. New Zealand Veterinary Journal 61, 87–97.
| Effects of novel and wild-type endophytes in perennial ryegrass on cow health and production.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC38bgsVWnsA%3D%3D&md5=1af96dc9336cfe3dac4388cd1d7a145dCAS | 22913546PubMed |
Tor-Agbidye J, Blythe LL, Craig AM (2001) Correlation of endophyte toxins (ergovaline and lolium B) with clinical disease: fescue foot and perennial ryegrass staggers. Veterinary and Human Toxicology 43, 140–146.
