Occurrence of Alkaloids in Grass Seeds Symbiotic With Vertically-Transmitted Epichloë Fungal Endophytes and Its Relationship With Antioxidants

Abstract

Host organisms can acquire new functional traits through symbiosis. Seed-transmitted Epichloë fungal endophytes are known to protect host plants against herbivores and increase tolerance to abiotic stresses by alkaloids and antioxidants, respectively (currencies of mutualism). Whereas, alkaloids are fungal products with demonstrated effects at plant vegetative stage, few studies have focused on alkaloids in seeds. We assessed the occurrence of fungal alkaloids and determined their concentrations in seeds of two host grasses, Festuca rubra and Lolium multiflorum. Then, we sought for a relationship with the antioxidants tocochromanols and glutathione, which are involved in the control of oxidative stress. Different alkaloids were detected depending on the species and plant genotype. Most notably, loline alkaloids were not detected in F. rubra seeds, whereas ergovaline and peramine were absent in L. multiflorum. In F. rubra, ergovaline concentration was dependent on the maternal line in interaction with the production year, diminishing in seeds after 1 year of storage. The exposure of L. multiflorum plants to ozone had no effect on the seed concentration of lolines. There was a significant positive relationship between the concentrations of ergovaline and tocochromanols in both species, and between ergovaline concentration and E GSSG/2GSH (glutathione halfcell reduction potential) in RAB maternal line of F. rubra. These results suggest that alkaloid and antioxidants have a close association in seeds of host grasses, and that the alkaloid bioactivity could be related with the antioxidant capacity to control stress. This has important implications for the ecology of partner species, thus supporting its consideration for further research.

Ontogenetic and trans‐generational dynamics of a vertically transmitted fungal symbiont in an annual host plant in ozone‐polluted settings

“…High concentrations of endophyte-derived alkaloids have been determined in seed Justus et al, 1997;TePaske et al, 1993;Vazquez de Aldana et al, 2003). These alkaloids are proposed to play an ecological role, protecting grass seed and seedlings against granivores and herbivores (Gundel, Seal, et al, 2018;Hewitt et al, 2020;A. V. Stewart, 1985;Uchitel et al, 2011).…”

“…The concentration of endophyte-derived alkaloids may be directly related to the level of protection conferred by a particular endophyte genotype (Bastías et al, 2018;Wilkinson et al, 2000). However, factors that regulate the endophyte-derived alkaloid production have been mostly studied in green tissues of plants and scarcely in seed (Gundel et al, 2017;Gundel, Seal, et al, 2018). A positive correlation has been observed between the concentration of endophyte-derived alkaloids and endophyte mycelial concentration in vegetative tissues of tall fescue (S. arundinaceus) and perennial ryegrass (Lolium perenne L.) (Easton, Latch, Tapper, & Ball, 2002;Keogh, Tapper, & Fletcher, 2010;Rasmussen et al, 2007); a relationship that can be shifted if plants grow under high concentrations of CO 2 (Ryan et al, 2014).…”

“…In addition, there is a strong genetic component controlling the survival of endophytes in seed, explaining some of the observed differences in endophyte status within grass populations (Gundel et al, 2010;Hill & Roach, 2009;Tian et al, 2013). Although the majority of studies investigating endophyte-derived alkaloids are concerned with the vegetative plant, this function has also been linked to the protection of reproductive structures and the seed (Faeth, 2009;Finch, Pennell, Kerby, & Cave, 2016;Pennell et al, 2017;Uchitel, Omacini, & Chaneton, 2011), which can extend to protection of the developing seedling (Gundel, Rudgers, & Whitney, 2017;Gundel, Seal, et al, 2018;Justus, Witte, & Hartmann, 1997;Ruppert, Matthew, McKenzie, & Popay, 2017;A. V. Stewart, 1985).…”

“…V. Stewart, 1985). Recent work has focused on the effects of the environment explored by mother plants on endophyte transmission and alkaloid production (Gundel et al, 2017;Gundel, Seal, et al, 2018).…”

“…Despite its implication for seed ecology, no information exists on the factors that affect alkaloid concentrations in seed (Gundel et al, 2017;Gundel, Seal, et al, 2018). In the plant, however, the concentrations of endophyte mycelia and alkaloids follow the seasonal plant growth, although different alkaloids can peak at slightly different stages (Bluett, Thom, Clark, Macdonald, & Minneé, 2005;.…”