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Distribution and Accumulation of the Mycotoxin Lolitrem B in Neotyphodium lolii- Infected Perennial Ryegrass

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Abstract

The symbiotic relationship between perennial ryegrass and its endophytic fungus, Neotyphodium lolii, is of considerable agronomic significance in New Zealand. Livestock ingesting N. lolii-infected perennial ryegrass may succumb to a neuromuscular condition, ryegrass staggers, the probable cause of which has been identified as the endophyte-produced indole–diterpenoid mycotoxin lolitrem B. The effects of plant component, plant reproductive development, and plant management (clipping) on the concentration and accumulation of lolitrem B were investigated. Eight different naturally occurring perennial ryegrass–N. lolii associations were cloned. They were either trimmed regularly to maintain their vegetative state (V clones) or not trimmed at all to enable full plant reproductive development (R clones). At times that corresponded approximately with the start, middle, and end of the plant reproductive phase, V and R clones of each grass–endophyte association were destructively harvested. After dissection into a number of plant components, harvested material was analyzed for lolitrem B content by HPLC. Analyses were also performed on all clippings taken from the V clones. Highest lolitrem B concentrations in vegetative parts were found in older leaf sheaths and dead leaves. Towards the end of the plant reprodutive phase, dead leaves also contained a large proportion of the total lolitrem B content of the V clones. The highest concentration of lolitrem B was found in the seed, which accounted for nearly 60% of the total quantity in R clones. Leaf blades, young leaf sheaths, roots, and crowns generally contained low to moderate concentrations. In late spring, mean concentrations in R and V clones were similar. By the time mature seed was present (mid-summer), mean concentrations in R clones were three times higher than in V clones. This difference was attributed largely to the contribution by the seed in the R clones. The implications of these findings in relation to ryegrass staggers in livestock are discussed.

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REFERENCES

  • AGEE, C. S., and HILL, N. S. 1994. Ergovaline variability in Acremonium-infected tall fescue due to environment and plant genotype. Crop. Sci. 34:221–226.

    Google Scholar 

  • BALL, O. J.-P. 1994. Interrelationships between perennial ryegrass (Lolium perenne), the endophytic fungus Neotyphodium lolii and black beetle (Heteronychus arator). PhD thesis. Department of Biological Sciences, University of Waikato, Hamilton, New Zealand.

  • BALL, O. J.-P., PRESTIDGE, R. A., and SPROSEN, J. M. 1995. Interrelationships between Acremonium lolii, peramine, and lolitrem B in perennial ryegrass. Appl. Environ. Microbiol. 61(4):1527–1533.

    Google Scholar 

  • BALL, O. J.-P., BARKER, G. M., PRESTIDGE, R. A., and LAUREN, D. R. 1997. Distribution and accumulation of the alkaloid peramine in Neotyphodium lolii-infected perennial ryegrass. J. Chem. Ecol. 23:1419–1434.

    Google Scholar 

  • BELESKY, D. P., STRINGER, W. C., and PLATTNER, R. D. 1989. Influence of endophyte and water regime upon tall fescue accessions. II. Pyrrolizidine and ergopeptine alkaloids. Ann. Bot. 64:343–349.

    Google Scholar 

  • BUSH, L. P., CORNELIUS, P. L., BUCKNER, R. C., VARNEY, S. R., CHAPMAN, R. A., BURRUS, II, P. B., KENNEDY, C. W., JONES, T. A., and SAUNDERS, M. J. 1982. Association of N-acetyl loline and N-formyl loline with Epichloe typhina in tall fescue. Crop Sci. 22:941–943.

    Google Scholar 

  • BUSH, L. P., FANNIN, F. F., SIEGEL, M. R., DAHLMAN, D. L., and BURTON, H. R. 1993. Chemistry, occurrence and biological effects of saturated pyrrolizidine alkaloids associated with endophyte-grass interactions. Agric. Ecosyst. Environ. 44:81–102.

    Google Scholar 

  • CUNNINGHAM, I. J., and HARTLEY, W. J. 1959. Ryegrass staggers. N.Z. Vet J. 7:1–7.

    Google Scholar 

  • DAVIES, E., LANE, G. A., LATCH, G. C. M., TAPPER, B. A., GARTHWAITE, I., TOWERS, N. R., FLETCHER, L. R., and POWNALL, D. B. 1993. Alkaloid concentrations in field-grown synthetic perennial ryegrass endophyte associations, pp. 72–76, in D. E. Hume, G. C. M. Latch, and H. S. Easton (eds.). Proceedings of the Second International Symposium on Acremonium/Grass Interactions. AgResearch, Palmerston North, New Zealand.

    Google Scholar 

  • DI MENNA, M. E., MORTIMER, P. H., PRESTIDGE, R. A., HAWKES, A. D., and SPROSEN, J. M. 1992. Lolitrem B concentrations, counts of Acremonium lolii hyphae, and the incidence of ryegrass staggers in lambs on plots of Acremonium lolii-infected perennial ryegrass. N.Z. J. Agric. Res. 35:211–217.

    Google Scholar 

  • DYMOCK, J. J., PRESTIDGE, R. A., and ROWAN, D. D. 1989. The effects of lolitrem B on Argentine stem weevil larvae. Proc. N.Z. Weed Pest Control Conf. 42:73–75.

    Google Scholar 

  • EVEREST, P. G. 1983. Ryegrass staggers: An overview of the north Canterbury situation and possible costs to the farmer. Proc. N.Z. Grassl. Assoc. 44:228–229.

    Google Scholar 

  • FLETCHER, L. R., and PIPER, E. 1990. Some factors besides Acremonium lolii which influence ryegrass staggers in grazing stock, pp. 216–220, in S. S. Quisenberry and R. E. Joost (eds.). Proceedings of the First International Symposium on Acremonium/Grass Interactions. Louisiana Agricultural Experiment Station, Baton Rouge, Louisiana.

    Google Scholar 

  • GALLAGHER, R. T., SMITH, G. S., DI MENNA, M. E., and YOUNG, P. W. 1982. Some observations on neurotoxin production in perennial ryegrass. N.Z. Vet. J. 30:203–204.

    Google Scholar 

  • GALLAGHER, R. T., HAWKES, A. D., STEYN, P. S., and VLEGGAAR, R. 1984. Tremorgenic neurotoxins from perennial ryegrass causing ryegrass staggers disorder of livestock: Structure elucidation of lolitrem B. J. Chem. Soc. Chem. Commun. (London) 1984:614–616.

    Google Scholar 

  • GALLAGHER, R. T., HAWKES, A. D., and STEWART, J. M. 1985. Rapid determination of the neurotoxin lolitrem B in perennial ryegrass by high-performance liquid chromatography with fluorescence detection. J. Chromatogr. 321:217–226.

    Google Scholar 

  • GALLAGHER, R. T., SMITH, G. S., and SPROSEN, J. M. 1987. The distribution and accumulation of lolitrem B neurotoxin in developing perennial ryegrass plants. Proc. A.A.A.P. Anim. Sci. Cong. 4:404.

    Google Scholar 

  • HEWETT, R. L. 1983. Breeding for resistance to ryegrass staggers, the inflation-proof long-term solution? Proc. N.Z. Grassl. Assoc. 44:244–247.

    Google Scholar 

  • KEOGH, R. G. 1973. Induction and prevention of ryegrass staggers in grazing sheep. N.Z. J. Exp. Agric. 1:55–57.

    Google Scholar 

  • KEOGH, R. G. 1978. Development and control of ryegrass staggers in sheep. Proc. N.Z. Soc. Anim. Prod. 38:47–52.

    Google Scholar 

  • KEOGH, R. G., and TAPPER, B. A. 1993. Acremonium lolii, lolitrem B, and peramine concentrations within vegetative tillers of perennial ryegrass, pp. 81–84, in D. E. Hume, G. C. M. Latch and H. S. Easton (eds.). Proceedings of the Second International Symposium on Acremoniuml/Grass Grass Interactions. AgResearch, Palmerston North, New Zealand.

    Google Scholar 

  • KNOCH, T. R., FAETH, S. H., and ARNOTT, D. L. 1993. Endophytic fungi alter foraging and dispersal by desert seed-harvesting ants. Oecologia 95:470–473.

    Google Scholar 

  • MORTIMER, P. H., and DI MENNA, M. E. 1985. Interactions of Lolium endophyte on pasture production and perennial ryegrass staggers disease, pp. 149–158, in J. Lacey (ed.). Trichothecenes and Other Mycotoxins. Wiley, New York.

    Google Scholar 

  • MUSGRAVE, D. R. 1984. Detection of an endophytic fungus of Lolium perenne using enzyme-linked immunosorbent assay (ELISA). N.Z. J. Agric. Res. 27:283–288.

    Google Scholar 

  • PRESTIDGE, R. A., and GALLAGHER, R. T. 1985. Lolitrem B—a stem weevil toxin isolated from Acremonium-infected ryegrass. Proc. N.Z. Weed Pest Control Conf. 38:38–40.

    Google Scholar 

  • PRESTIDGE, R. A., and GALLAGHER, R. T. 1988. Acremonium endophyte in perennial ryegrass, ryegrass staggers in lambs, and growth rate of Argentine stem weevil larvae, pp. 229–235, in P. P. Stahle (ed.). Proceedings of the Fifth Australasian Conference on Grassland Invertebrate Ecology: Melbourne, Australia. D and D Printing, Victoria, Australia.

    Google Scholar 

  • ROTTINGHAUS, G. E., GARNER, G. B., CORNELL, C. N., and ELLIS, J. L. 1991. HPLC method for quantitating ergovaline in endophyte-infested tall fescue: Seasonal variation of ergovaline levels in stems with leaf sheaths, leaf blades, and seed heads. J. Agric. Food Chem. 39:112–115.

    Google Scholar 

  • STEEL, R. G. D., and TORRIE, J. H. 1980. Principles and Procedures of Statistics. McGraw-Hill, New York.

    Google Scholar 

  • STEWART, A. V. 1985. Perennial Ryegrass seedling resistance to Argentine stem weevil. N.Z. J. Agric. Res. 28:403–407.

    Google Scholar 

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Authors and Affiliations

  1. AgResearch, Grasslands Research Centre, Private Bag 11008, Palmerston North, New Zealand

    O. J.-P. Ball

  2. Landcare Research, Private Bag 3127, Hamilton, New Zealand

    G. M. Barker

  3. AgResearch, Ruakura Agricultural Research Centre, Private Bag 3123, Hamilton, New Zealand

    R. A. Prestidge & J. M. Sprosen

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  1. O. J.-P. Ball
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  2. G. M. Barker
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  3. R. A. Prestidge
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  4. J. M. Sprosen
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Ball, O.JP., Barker, G.M., Prestidge, R.A. et al. Distribution and Accumulation of the Mycotoxin Lolitrem B in Neotyphodium lolii- Infected Perennial Ryegrass. J Chem Ecol 23, 1435–1449 (1997). https://doi.org/10.1023/B:JOEC.0000006474.44100.17

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  • DOI: https://doi.org/10.1023/B:JOEC.0000006474.44100.17

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