Skip to main content
SpringerLink
Log in

Fungal Alkaloid Occurrence in Endophyte-Infected Perennial Ryegrass during Seedling Establishment

  • Published:
Journal of Chemical Ecology Aims and scope Submit manuscript

A Correction to this article was published on 27 March 2020

This article has been updated

Abstract

The symbiotic Epichloë festucae var. lolii endophyte produces alkaloids which can provide its host grass, perennial ryegrass (Lolium perenne L), with a selective advantage in both natural and agricultural managed ecosystems. This study focuses on understanding the alkaloid concentrations that occur in endophyte-infected perennial ryegrass during the early establishment phase. In a glasshouse experiment fungal alkaloid concentrations (peramine, lolitrem B, ergovaline, and epoxy-janthitrems) were measured in perennial ryegrass seedlings infected with E. festucae var. lolii proprietary strains AR1, AR37, NEA2, and NZ common toxic for 69 days after sowing. The endophyte becomes metabolically active, starting alkaloid production, as early as 6 days after sowing. Alkaloid concentrations peaked in 8- to 10- day-old seedlings due to a seedling growth slowdown. This study provides data showing that the loss of insect protection in endophyte-infected seedlings is linked to a reduction in chemical defence after seed-stored, maternally synthesised alkaloids are diluted by seedling dry matter accumulation.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

Change history

  • 27 March 2020

    The original version of this article unfortunately contained a mistake. There is a mistake in the affiliation section and Figure 6. The correct affiliation and Figure 6 are shown here.

References

  • Anslow R (1962) A quantitative analysis of germination and early seedling growth in perennial ryegrass. Grass Forage Sci 17:260–263

    Article  Google Scholar 

  • Arechavaleta M, Bacon CW, Plattner RD, Hoveland CS, Radcliffe DE (1992) Accumulation of ergopeptide alkaloids in symbiotic tall fescue grown under deficits of soil water and nitrogen fertilizer. Applied and Environmental Microbiology 58:857–861

    Article  CAS  Google Scholar 

  • Bacon CW, Siegel MR (1988) Endophyte parasitism of tall fescue. Journal of Production Agriculture 1:45–55

    Article  Google Scholar 

  • Ball OJ-P, Prestidge RA, Sprosen JM (1993) Effect of plant age and endophyte viability on peramine and lolitrem B concentration in perennial ryegrass seedlings. In: Hume DE, Latch GCM, Easton HS (eds) Proceedings of the 2nd international symposium on Acremonium/grass interactions, vol 2. Palmerston North, New Zealand, pp 63–66

    Google Scholar 

  • Ball OJP, Barker GM, Prestidge RA, Lauren DR (1997a) Distribution and accumulation of the alkaloid peramine in Neotyphodium lolii-infected perennial ryegrass. Journal of Chemical Ecology 23:1419–1434

    Article  CAS  Google Scholar 

  • Ball OJP, Barker GM, Prestidge RA, Sprosen JM (1997b) Distribution and accumulation of the mycotoxin lolitrem B in Neotyphodium lolii-infected perennial ryegrass. Journal of Chemical Ecology 23:1435–1449

    Article  CAS  Google Scholar 

  • Ball OJP, Christensen MJ, Prestidge RA (1994) Effect of selected isolates of Acremonium endophyte on adult black beetle (Heteronychus arator) feeding. In: Popay A (ed) Proceedings of the 47th New Zealand plant protection conference, New Zealand Plant Protection Society, 9–11 august, vol 47. Rotorua, New Zealand, pp 227–231

    Google Scholar 

  • Bluett SJ, Thom ER, Clark DA, Macdonald KA, Minnee EMK (2005a) 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

    Article  Google Scholar 

  • Bluett SJ, Thom ER, Clark DA, Waugh CD (2005b) Effects of a novel ryegrass endophyte on pasture production, dairy cow milk production and calf liveweight gain. Collingwood, Australia

    Book  Google Scholar 

  • Bultman TL, Bell GD (2003) Interaction between fungal endophytes and environmental stressors influences plant resistance to insects. Oikos 103:182–190. https://doi.org/10.1034/j.1600-0706.2003.11574.x

    Article  Google Scholar 

  • Bultman TL, McNeill M, Krueger K, de Nicolo G, Popay AJ, Hume DE, Mace WJ, Fletcher LR, Koh YM, Sullivan TJ (2018) Complex interactions among sheep, insects, grass, and fungi in a simple New Zealand grazing system. J Chem Ecol 44:957–964

    Article  CAS  Google Scholar 

  • Card SD, Faville MJ, Simpson WR, Johnson RD, Voisey CR, De Bonth ACM, Hume DE (2014) Mutualistic fungal endophytes in the Triticeae – survey and description microbial ecology

  • Christensen M, Voisey C (2007) The biology of the endophyte/grass partnership. In: Popay a, Thom ER (eds) 6th international symposium on fungal Endophytes of grasses, vol grassland research and practice series no. 13. New Zealand grasslands association, Christchurch, New Zealand, pp 123-133

  • Christensen MJ et al (2008) Epichloë endophytes grow by intercalary hyphal extension in elongating grass leaves. Fungal Genet Biol 45:84–93

    Article  Google Scholar 

  • Christensen MJ, Bennett RJ, Schmid J (2002) Growth of Epichloe/Neotyphodium and p-endophytes in leaves of Lolium and Festuca grasses. Mycological Research 106:93–106

    Article  Google Scholar 

  • Clay K (1988) Fungal endophytes of grasses: a defensive mutualism between plants and fungi Ecology:10–16

  • di Menna ME, Mortimer PH, Prestidge RA, Hawkes AD, Sprosen JM (1992) Lolitrem B concentrations, counts of Acremonium lolii hyphae, and the incidence of ryegrass staggers in lambs on plots of A. lolii-infected perennial ryegrass. New Zealand journal of agricultural research 35:211–217

    Article  Google Scholar 

  • Faeth SH, Bush LP, Sullivan TJ (2002) Peramine alkaloid variation in Neotyphodium-infected Arizona fescue: Effects of endophyte and host genotype and environment. Journal of Chemical Ecology 28:1511–1526

    Article  CAS  Google Scholar 

  • Faville M, Koulman A, Briggs L, Cao M, Podmore C (2007) Abraham D Exploring endophyte compatibility in perennial ryegrass. In: Proceedings of the 6th International Symposium on Fungal Endophytes of Grasses’. Christchurch, New Zealand. Grassland Research and Practice Series 13:143–146

    Google Scholar 

  • Fuchs B, Krischke M, Mueller MJ, Krauss J (2013) Peramine and lolitrem B from endophyte-grass associations cascade up the food chain. Journal of chemical ecology 39:1385–1389

    Article  CAS  Google Scholar 

  • Glassey C, Roach C, Strahan M, McLean N (2010) Dry matter yield, pasture quality and profit on two Waikato dairy farms after pasture renewal. In: Proceedings of the New Zealand Grassland Association, 72. pp 91–96

  • Guerre P (2015) Ergot alkaloids produced by endophytic fungi of the genus. Epichloë toxins 7:773–790

    Article  CAS  Google Scholar 

  • Gundel PE et al (2018) Occurrence of alkaloids in grass seeds symbiotic with vertically-transmitted Epichloë fungal endophytes and its relationship with antioxidants. Frontiers in Ecology and Evolution 6:211

    Article  Google Scholar 

  • Hennessy LM, Popay AJ, Finch SC, Clearwater MJ, Cave VM (2016) Temperature and Plant Genotype Alter Alkaloid Concentrations in Ryegrass Infected with an Epichloë Endophyte and This Affects an Insect Herbivore Frontiers in Plant Science 7

  • Johnson LJ et al. (2013) The exploitation of epichloae endophytes for agricultural benefit fungal diversity 60:171-188 doi:https://doi.org/10.1007/s13225-013-0239-4

  • Knoch TR, Faeth SH, Arnott DL (1993) Endophytic fungi alter foraging and dispersal by desert seed-harvesting ants. Oecologia 95:470–473. https://doi.org/10.1007/bf00317429

    Article  PubMed  Google Scholar 

  • Leuchtmann A, Bacon CW, Schardl CL, White JFJ, Tadych M (2014) Nomenclatural realignment of Neotyphodium species with genus Epichloë. Mycologia:106. https://doi.org/10.3852/13-251

  • Lucero JE, Callaway RM (2018) Granivory from native rodents and competition from an exotic invader strongly and equally limit the establishment of native grasses. Oecologia 186:1043–1053

    Article  Google Scholar 

  • Madej CW, Clay K (1991) Avian seed preference and weight loss experiments: the effect of fungal endophyte-infected tall fescue seeds. Oecologia 88:296–302

    Article  Google Scholar 

  • Mitchell ML, Virgona J, Jacobs JL, Kemp D (2014) Population biology of Microlaena stipoides in a south-eastern Australian pasture. Crop and Pasture Science 65:767–779

    Article  Google Scholar 

  • Moate PJ et al (2012) Effects of wild-type, AR1 and AR37 endophyte-infected perennial ryegrass on dairy production in Victoria. Australia Animal Production Science 52:1117–1130. https://doi.org/10.1071/AN12126

    Article  CAS  Google Scholar 

  • Moore JR, Pratley J, Mace W, Weston LA (2015) Variation in alkaloid production from genetically diverse Lolium accessions infected with Epichloë species journal of agricultural and food chemistry

  • Popay A, Marshall S, Baltus J (2000a) Endophyte infection influences disappearance of perennial ryegrass seed. In: Zydenbos SM (ed) New Zealand plant protection, 7–10 August, vol 53. Christchurch, New Zealand, pp 398–405

    Google Scholar 

  • Popay AJ, Baltus J, Pennell C (2000b) Insect resistance in perennial ryegrass infected with toxin-free Neotyphodium endophytes. In: fourth international Neotyphodium/grass interactions symposium, Soest, Germany, pp 187–193

  • Popay AJ, Bonos SA (2005) Biotic responses in Endophytic grasses. In: Roberts CA, West CP, Spiers DE (eds) Neotyphodium in cool-season grasses. Blackwell Publishing, Ames, pp 163–185

    Chapter  Google Scholar 

  • Popay AJ, Hume DE (2011) Endophytes improve ryegrass persistence by controlling insects. In: Mercer CF (ed) Pasture persistence symposium. Grassland research and practice series no. 15, vol 15. New Zealand Grassland Association, Dunedin, pp 149–156

  • Popay AJ, Wyatt RT (1995) Resistance to argentine stem weevil in perennial ryegrass infected with endophytes producing different alkaloids. In: Popay a (ed) New Zealand plant protection conference, vol 48. 8-10 august, Hastings, pp 229-236

  • Qawasmeh A (2012) Biochemical consequences of endophytic fungi–grass mutualism. Charles Sturt University

  • 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. Methods in Molecular Biology 860:213–226

    Article  CAS  Google Scholar 

  • Rasmussen S et al (2006) High nitrogen supply and carbohydrate content reduce fungal endophyte and alkaloid concentration in Lolium perenne. New Phytol 173:787–797

    Article  CAS  Google Scholar 

  • Rowan DD, Dymock JJ, Brimble MA (1990) Effect of fungal metabolite peramine and analogs on feeding and development of Argentine stem weevil (Listronotus bonariensis). Journal of Chemical Ecology 16:1683–1695

    Article  CAS  Google Scholar 

  • Ruppert KG, Matthew C, McKenzie CM, Popay AJ (2017) Impact of Epichloë endophytes on adult Argentine stem weevil damage to perennial ryegrass seedlings. Entomologia Experimentalis et Applicata 163:328–337

    Article  CAS  Google Scholar 

  • Ryan G, Rasmussen S, Parsons A, Newman J (2015) The effects of carbohydrate supply and host genetic background on Epichloë endophyte and alkaloid concentrations in perennial ryegrass. Fungal Ecology 18:115–125

    Article  Google Scholar 

  • Schardl CL, Leuchtmann A, Chung KR, Penny D, Siegel MR (1997) Coevolution by common descent of fungal symbionts (Epichloë spp.) and grass hosts. Mol Biol Evol 14:133–143

    Article  CAS  Google Scholar 

  • Simpson WR, Schmid J, Singh J, Faville MJ, Johnson RD (2012) A morphological change in the fungal symbiont Neotyphodium lolii induces dwarfing in its host plant Lolium perenne. Fungal Biology 116:234–240. https://doi.org/10.1016/j.funbio.2011.11.006

    Article  PubMed  CAS  Google Scholar 

  • 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. https://doi.org/10.1016/j.phytochem.2004.11.021

    Article  PubMed  CAS  Google Scholar 

  • Steinfeld H, Gerber P, Wassenaar T, Castel V, Rosales M, Rosales M, de Haan C (2006) Livestock's long shadow: environmental issues and options. Food & Agriculture Org.,

  • Stewart AV (1985) Perennial ryegrass seedling resistance to argentine stem weevil. N Z J Agric Res 28:403–407

    Article  Google Scholar 

  • Sugawara K, Ohkubo H, Tsukiboshi T (2007) Distribution and morphology of Neotyphodium endophytes in apical meristems of host plants as observed using differential interference contrast microscopy. In: Proceedings of the 6th International Symposium on Fungal Endophytes of Grasses, pp 139–141

  • Tan YY, Spiering MJ, Scott V, Lane GA, Christensen MJ, Schmid J (2001) In planta regulation of extension of an endophytic fungus and maintenance of high metabolic rates in its mycelium in the absence of apical extension. Applied and Environmental Microbiology 67:5377–5383

    Article  CAS  Google Scholar 

  • VSN International (2018) GenStat for windows 18th edition. VSN International, Hempel Hempstread, UK

  • Wang J et al. (2014) Development and implementation of a multiplexed single nucleotide polymorphism genotyping tool for differentiation of ryegrass species and cultivars molecular breeding 33:435-451

  • Zhang W, Card SD, Mace WJ, Christensen MJ, McGill CR, Matthew C (2017) Defining the pathways of symbiotic Epichloë colonization in grass embryos with confocal microscopy. Mycologia 109:153–161

    Article  CAS  Google Scholar 

  • Zhang W, Mace WJ, Matthew C, Card SD (2019) The impact of endophyte infection, seed aging and imbibition on selected sugar metabolite concentrations in seed journal of agricultural and food chemistry

Download references

Acknowledgements

The authors would like to thank New Zealand Agriseeds and Alan Stewart from PGG Wrightson Seeds for providing seed material. Special gratitude goes to the T.R. Ellett Agricultural Research Trust for funding.

Author information

Author notes

  1. Katrin G. Hewitt

    Present address: The New Zealand Institute for Plant and Food Research Limited (Plant & Food Research), Physiological Chemistry, Ruakura, Private Bag 3230, Waikato Mail Centre, Hamilton, 3240, New Zealand

Authors and Affiliations

  1. AgResearch Ltd, Forage Improvement, Grasslands Research Centre, Private Bag 11008, Palmerston North, 4442, New Zealand

    Wade J. Mace

  2. Plant & Food Research, Data Science, 412 No 1 Road, RD 2, Te Puke, 3182, New Zealand

    Catherine M. McKenzie

  3. School of Agriculture and Environment, Massey University, Private Bag 11-222, Palmerston North, 4442, New Zealand

    Cory Matthew

  4. AgResearch Ltd, Biocontrol & Biosecurity, Ruakura Research Private Bag 3123, Hamilton, 3240, New Zealand

    Alison J. Popay

  5. AgResearch Ltd, Biocontrol & Biosecurity, Grasslands Research Centre, Private Bag 11008, Palmerston North, 4442, New Zealand

    Katrin G. Hewitt

Authors
  1. Katrin G. Hewitt
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Wade J. Mace
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Catherine M. McKenzie
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Cory Matthew
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Alison J. Popay
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

KGH, WJM, AJP, CMcK, CM conceived and designed the research. KGH conducted the experiment as part of her Master of Science (Research). CMcK analysed the data. KGH wrote the majority of the manuscript. All authors read and approved the manuscript.

Corresponding author

Correspondence to Katrin G. Hewitt.

Additional information

The original version of this article was revised: The original version of this article unfortunately contained a mistake. There is a mistake in the affiliation section and Figure 6. The correct affiliation and Figure 6 are shown here.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Hewitt, K.G., Mace, W.J., McKenzie, C.M. et al. Fungal Alkaloid Occurrence in Endophyte-Infected Perennial Ryegrass during Seedling Establishment. J Chem Ecol 46, 410–421 (2020). https://doi.org/10.1007/s10886-020-01162-w

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10886-020-01162-w

Keywords

Search

Navigation