Alkaloid Variation Among Epichloid Endophytes of Sleepygrass (Achnatherum robustum) and Consequences for Resistance to Insect Herbivores

Abstract

Epichloid endophytes are well known symbionts of many cool-season grasses that may alleviate environmental stresses for their hosts. For example, endophytes produce alkaloid compounds that may be toxic to invertebrate or vertebrate herbivores. Achnatherum robustum, commonly called sleepygrass, was aptly named due to the presence of an endophyte that causes toxic effects to livestock and wildlife. Variation in alkaloid production observed in two A. robustum populations located near Weed and Cloudcroft in the Lincoln National Forest, New Mexico, suggests two different endophyte species are present in these populations. Genetic analyses of endophyte-infected samples revealed major differences in the endophyte alkaloid genetic profiles from the two populations, which were supported with chemical analyses. The endophyte present in the Weed population was shown to produce chanoclavine I, paspaline, and terpendoles, so thus resembles the previously described Epichloë funkii. The endophyte present in the Cloudcroft population produces chanoclavineI, ergonovine, lysergic acid amide, and paspaline, and is an undescribed endophyte species. We observed very low survival rates for aphids feeding on plants infected with the Cloudcroft endophyte, while aphid survival was better on endophyte infected plants in the Weed population. This observation led to the hypothesis that the alkaloid ergonovine is responsible for aphid mortality. Direct testing of aphid survival on oat leaves supplemented with ergonovine provided supporting evidence for this hypothesis. The results of this study suggest that alkaloids produced by the Cloudcroft endophyte, specifically ergonovine, have insecticidal properties.

Ergot Alkaloids of the Family Clavicipitaceae

“…Epichloë species, which grow endobiotically and are often seed-transmitted in cool-season grasses (Poaceae, subfamily Poöideae), can be a source of various ergot alkaloids that cause important toxic syndromes in livestock (Chen et al 2015; Klotz 2015; Shymanovich et al 2015; Thompson and Stuedemann 1993). Periglandula species, which are epibiotic symbionts on buds and leaf surfaces of morning glories (Convolvulaceae, tribe Ipomoeae), produce diverse ergot alkaloids (Beaulieu et al 2015).…”

“…This seems to contradict the common paradigm that systems evolve toward greater complexity, but these simpler lysergic acid amides may have been selectively favored in some systems because they are less costly for the fungus to produce. Although there is overlap of symptoms associated with simpler and complex lysergic acid amides, mammalian grazers that ingest ergopeptines can exhibit acute toxicoses, whereas those ingesting the simpler lysergic acid amides present in sleepy grass ( Achnatherum robustum ) and drunken horse grass ( Achnatherum inebrians ) exhibit inebriation and are deterred from future grazing of these plants (Chen et al 2015; Shymanovich et al 2015). …”

Antimicrobial fungal endophytes from the botanical medicine goldenseal ( Hydrastis canadensis )

“…The measured quantity of 991 ppm alternariol monomethyl ether in the H. canadensis seeds is in the concentration range reported for metabolites known to be ecologically important, such as the ergot and loline alkaloids produced by fungal endophytes of native grasses (Jarmusch et al, 2016; Shymanovich et al, 2014). Ergot and loline alkaloid alkaloids help protect grasses from insect herbivores (Bush et al, 1997).…”

Effect of Endophyte Infection and Clipping Treatment on Resistance and Tolerance of Achnatherum sibiricum

“…In Arizona fescue, only a low concentration of peramine was produced, and infected plants did not show significant resistance to Xanthippus corallipes , Melanoplus femurrubrum , and Acromyrmex versicolor (Saikkonen et al, 1999; Tibbets and Faeth, 1999). Shymanovich et al (2015) observed different aphid resistance of sleepy grass in different populations, with very low survival rates for the aphids feeding on plants infected with the Cloudcroft endophyte, whereas aphid survival was better on EI plants in the Weed population. In addition, they suggested that the alkaloid ergonovine was responsible for aphid mortality.…”