Understanding Endophytes: The history and morphology of endophytes and comparison of endophyte-infected tall fescue in the US

Tall fescue is a dominant grass across the US

Tall fescue is a deep-rooted, persistent perennial grass that is considered high-quality forage for livestock. Tall fescue originated from Europe and was likely brought here by early European settlers. Kentucky 31 (KY-31), infamous fescue cultivar released in 1942, is well adapted to the eastern states and has become a dominant grass that filled a void in the landscape and a need for farmers. Yet by the early 1950s poor animal performance, with lower-than-expected average daily gains, low conception rates, lower milk production, poor heat tolerance, and vasoconstriction that resulted in loss of hooves and tails had been observed in cattle (Stuedemann and Hoveland 1988). Pregnant mares consuming KY-31 tall fescue have been reported with reduced milk production, prolonged gestation (up to 27 days longer), abortions, and thickened placentas (Cross et al 1995, Blodgett 2001).

Discovering an endophyte and the cause of fescue toxicosis

In the 1970s a USDA scientist Charles Bacon observed an endophyte (endo=inside, phyte=plant) associated in fescue pastures that correlated with fescue toxicosis (Bacon et al 1977). This endophyte is a fungus that remains inconspicuous in its host, colonizing the above ground tissue and is also transmitted to the next generation via the seed (Fig. 1). As our knowledge of this fungus improved it underwent several name changes (Epichloë typhina, Acremonium coenophialum, Neotyphodium coenophialum), but is now known as Epichloë coenophiala (Leutchmann et al 2014). What makes tall fescue toxic to livestock is not simply the endophyte but the fact that the endophyte can produce toxic compounds known as ergot alkaloids, such as ergovaline (Fig. 2A) (Porter et al 1981). These mycotoxins can interfere with the receptors such as those for dopamine and serotonin (Klotz 2015).

Figure 1. Endophyte in tall fescue detected by microscopy. (A) Sample from a the pseudostem of a fescue leaf sheath. The endophyte is stained blue and seen as the convoluted vertical lines. The outline of the plant cells is not visible. (B) Sample from an endophyte-infected fescue seed. The endophyte is the blue squiggly lines. The plant aleurone layer is visible as blue stained irregular shapes.

How are ergot alkaloids produced?

The endophyte found in Kentucky 31 has a set of genes (genetic machinery) that encode the biosynthetic steps required to generate ergot alkaloids that cause livestock toxicity. Ergovaline (Fig.2A) is an ergot alkaloid that can be detected in KY-31 fescue pastures. Although produced by the fungus, production of ergot alkaloids can also respond to environmental and management triggers. As example, when nitrogen is applied to the field this can increase production of the ergot alkaloids. In addition, the various parts of the plant can also have different concentrations of ergot alkaloids. During the vegetative stage of fescue growth, the endophyte is predominantly in the leaf sheath and pseudostem of the plant and very little endophyte is present in the blade. This is a great reason to make sure E+ KY-31 isn’t overgrazed otherwise the livestock will be eating fescue with the highest amounts of endophyte and the highest concentration of ergot alkaloids, whereas the leaf blades can contain much lower levels (Takach et al 2012). Once the inflorescences start to develop, the endophyte starts to colonize the developing seed heads, which is a peak time for ergot alkaloid production (Smith et al 2009).

Figure 2. Structures of the compounds made by Epichloë species. (A) Ergovaline is an ergot alkaloid that is associated with fescue toxicosis of livestock. (B) Lolitrem B is an indole-diterpene associated with ryegrass staggers in livestock. (C) Peramine is a pryrrolpyrazine that acts as an insect feeding deterrent. (D) N-formylloline is a pyrrolizidine that has strong insecticidal properties.

Epichloë species produce other compounds that protect their host

It is easy to give tall fescue a bad name due to the production of ergot alkaloids, but these compounds are not the only ones produced by the Epichloë species. Other compounds, peramine (pyrrolopryazine), lolines, and indole diterpenes can also be produced by the fungus, which provide natural protection against some insects (Fig. 2) (Schardl et al 2013). In fact, there are strains of fescue endophytes that can produce some combination of all these compounds, including strains that aren’t able to make ergot alkaloids at all (Table 1). The endophyte strains that can’t produce ergot alkaloids don’t have the genes or genetic machinery required for production of ergot alkaloids (Takach and Young 2014). Identifying endophytes that are compatible with tall fescue but don’t make ergot alkaloids is one way to solve the fescue toxicosis problem (Young et al 2013). Several non-ergot alkaloid endophyte strains (Table 1) have now been identified in tall fescue that grows in the Mediterranean region. We use molecular tools to easily distinguish all of these endophyte strains.

Endophytes were the cause but can also be the solution

The initial solution to prevent fescue toxicosis was to develop endophyte-free (E-) tall fescue by removing the endophyte from the seed with heat and humidity or long-term storage. Unfortunately, these E- pastures were not as persistent as their endophyte-infected (E+) KY-31 counterparts, and within a few short years the E- stands are lost (Bouton et al 1993). It turns out the endophyte provides its host with persistence to insects (see the comments above about other compounds the endophyte makes), pathogens, drought, and some nutrient deficiency (Schardl et al 2023).

Figure 3. Average daily gains of cattle eating E+ KY-31 or the novel endophyte-infected (NE+) cultivars, Jesup MaxQ or Texoma MaxQ II that don’t produce ergot alkaloids. Adapted from Parish et al 2013.

Endophyte-free (E-) fescue wasn’t the solution but a group in New Zealand was able to create cultivars with naturally occurring endophytes that don’t produce ergot alkaloids (Table 1) but still retain host persistence (Johnson et al 2013). When tested on cattle, the animal performance was far superior to that of the E+ KY-31, where cattle grazing the new novel endophyte infected (NE+) cultivars, Jesup MaxQ and Texoma MaxQ II, had almost double the average daily gains than those on E+ KY-31 (Fig. 3) (Parish et al 2013). NE+ tall fescue is also a suitable forage for pregnant mares, as they performed as well as those grazing orchardgrass/Kentucky blue grass mix, showing no signs of fescue toxicity typically seen with E+ KY-31 (McDowell et al 2019).  In addition, the NE+ cultivar Texoma MaxQ II has been shown to be more desirable for beneficial dung beetle performance, which provides nutrients back into the soil (Shymanovich et al 2020).

Several non-ergot alkaloid producing endophytes have now been deployed in tall fescue cultivars that can be used for pasture renovation to combat fescue toxicosis. Information on the available NE+ tall fescue cultivars has been developed by Phipps et al 2021. Our understanding of fescue toxicosis and the cause has come a long way since it was first observed in the 1950s. An endophyte that was once considered the bane of fescue production has now been replaced with better endophyte strains (NE+ cultivars) and these new cultivars can provide all the benefits for retaining host persistence, without ergot alkaloid toxicity to grazing livestock.

~ Dr. Carolyn Young, Department of Entomology and Plant Pathology, North Carolina State University, Raleigh, NC | Email: cyoung6@ncsu.edu | Twitter: @KiwiYoung. Proceedings written for the Equines and Endophytes Workshop, Lexington, KY January 25, 2023

References

  • Bacon CW, Porter JK, Robbins JD, Luttrell ES. 1977. Epichloe typhina from toxic tall fescue grasses. Applied and Environmental Microbiology. 34:576-81.
  • Blodgett DJ. 2001. Fescue toxicosis. Veterinary Clinics of North America: Equine Practice. 17:567-77.
  • Bouton JH, Gates RN, Belesky DP, Owsley M. 1993. Yield and persistence of tall fescue in the southeastern coastal plain after removal of its endophyte. Agronomy Journal. 85:52-5.
  • Cross DL, Redmond LM, Strickland JR. 1995. Equine fescue toxicosis: signs and solutions. Journal of Animal Science. 73:899-908.
  • Johnson LJ, de Bonth A, Briggs LR, Caradus JR, Finch SC, Fleetwood DJ, Fletcher LR, Hume DE, Johnson RD, Popay AJ, Tapper BA. 2013. The exploitation of epichloae endophytes for agricultural benefit. Fungal Diversity. 60:171-88.
  • Klotz JL. 2015. Activities and effects of ergot alkaloids on livestock physiology and production. Toxins. 7:2801-21.
  • Parish JA, Parish JR, Best TF, Boland HT, Young CA. 2013. Effects of selected endophyte and tall fescue cultivar combinations on steer grazing performance, indicators of fescue toxicosis, feedlot performance, and carcass traits. Journal of Animal Science. 91:342-55.
  • Phipps K, Talbott C, Newsome M, Harmon D, Poore M. 2021. https://content.ces.ncsu.edu/comparison-of-commercially-available-novel-endophyte-tall-fescue-forage-varieties
  • Porter JK, Bacon CW, Robbins JD, Betowski D. 1981. Ergot alkaloid identification in Clavicipitaceae systemic fungi of pasture grasses. Journal of Agricultural and Food Chemistry. 29:653-7.
  • Schardl CL, Afkhami ME, Gundel PE, Iannone LJ, Young CA, Creamer R, Cook DD, Berry D. 2023. Diversity of Seed Endophytes: Causes and Implications. InPlant Relationships pp. 83-132. Springer, Cham.
  • Schardl CL, Young CA, Pan J, Florea S, Takach JE, Panaccione DG, Farman ML, Webb JS, Jaromczyk J, Charlton ND, Nagabhyru P. 2013. Currencies of mutualisms: sources of alkaloid genes in vertically transmitted epichloae. Toxins. 5:1064-88.
  • Shymanovich T, Crowley G, Ingram S, Steen C, Panaccione DG, Young CA, Watson W, Poore M. 2020. Endophytes matter: Variation of dung beetle performance across different endophyte-infected tall fescue cultivars. Applied Soil Ecology. 152:103561.
  • Smith SR, Schwer L, Keene TC. 2009. Tall fescue toxicity for horses: Literature review and Kentucky’s successful Pasture Evaluation Program. Forage and Grazinglands.
  • Stuedemann JA, Hoveland CS. 1988. Fescue endophyte: History and impact on animal agriculture. Journal of Production Agriculture. 1:39-44.
  • Takach JE, Mittal S, Swoboda GA, Bright SK, Trammell MA, Hopkins AA, Young CA. 2012. Genotypic and chemotypic diversity of Neotyphodium endophytes in tall fescue from Greece. Applied and Environmental Microbiology. 78:5501-10.
  • Takach JE, Young CA. 2014. Alkaloid genotype diversity of tall fescue endophytes. Crop Science. 54:667-78.
  • Young CA, Hume DE, McCulley RL. 2013. Forages and pastures symposium: fungal endophytes of tall fescue and perennial ryegrass: pasture friend or foe? Journal of Animal Science. 91:2379-94.

The Alliance for Grassland Renewal is a national organization focused on enhancing the appropriate adoption of novel endophyte tall fescue technology through education, incentives, self-regulation and promotion.  For more resources or to learn more about the Alliance for Grassland Renewal, go to www.grasslandrenewal.org

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