Anti-herbivory defences delivered by Epichloë fungal endophytes: a quantitative review of alkaloid concentration variation among hosts and plant parts

Abstract

Background and aims: In the subfamily Poöideae (Poaceae), certain grass species possess anti-herbivore alkaloids synthesized by fungal endophytes that belong to the genus Epichloë (Clavicipitaceae). The protective role of these symbiotic endophytes can vary, depending on alkaloid concentrations within specific plant-endophyte associations and plant parts.

Methods: We conducted a literature review to identify articles containing alkaloid concentration data for various plant parts in six important pasture species, Lolium arundinaceum, Lolium perenne, Lolium pratense, Lolium multiflorum|Lolium rigidum and Festuca rubra, associated with their common endophytes. We considered the alkaloids lolines (1-aminopyrrolizidines), peramine (pyrrolopyrazines), ergovaline (ergot alkaloids) and lolitrem B (indole-diterpenes). While all these alkaloids have shown bioactivity against insect herbivores, ergovaline and lolitrem B are harmful for mammals.

Key results: Loline alkaloid levels were higher in the perennial grasses L. pratense and L. arundinaceum compared to the annual species L. multiflorum and L. rigidum, and higher in reproductive tissues than in vegetative structures. This is probably due to the greater biomass accumulation in perennial species that can result in higher endophyte mycelial biomass. Peramine concentrations were higher in L. perenne than in L. arundinaceum and not affected by plant part. This can be attributed to the high within-plant mobility of peramine. Ergovaline and lolitrem B, both hydrophobic compounds, were associated with plant parts where fungal mycelium is usually present, and their concentrations were higher in plant reproductive tissues. Only loline alkaloid data were sufficient for below-ground tissue analyses and concentrations were lower than in above-ground parts.

Conclusions: Our study provides a comprehensive synthesis of fungal alkaloid variation across host grasses and plant parts, essential for understanding the endophyte-conferred defence extent. The patterns can be understood by considering endophyte growth within the plant and alkaloid mobility. Our study identifies research gaps, including the limited documentation of alkaloid presence in roots and the need to investigate the influence of different environmental conditions.

Keywords: Symbiosis; defensive mutualism; grass; herbivory resistance; plant–endophyte interaction; plant–herbivore interaction; secondary metabolites.

Fig. 1.

Concentration of Epichloë-derived loline alkaloids in different plant–endophyte symbioses (indicated through host species name) and plant parts. The category ‘above-ground’ is used to aggregate all data from studies that did not define the tissue type, either vegetative or reproductive. Points around the boxplots are independent studies (N = 132). Loline alkaloids correspond to the sum of N-acetylnorloline (NANL), N-formylloline (NFL) and N-acetylloline (NAL). Asterisks denote significant effects of symbioses (S), plant part (P) or their interaction (S × P) as shown in Table 2. For vegetative and reproductive plant parts, distinct letters on boxplots indicate significant differences (P < 0.05) based on post-hoc multiple comparisons of means. *P < 0.05; **P < 0.01; ***P < 0.001. DW, dry weight.

Fig. 2.

Concentration of Epichloë-derived peramine alkaloid in different plant–endophyte symbioses (indicated through host species name) and plant parts. The category ‘above-ground’ is used to aggregate all data from studies that did not define the tissue type, either vegetative or reproductive. Points around the boxplots are independent studies (N = 97). Asterisks denote significant effects of symbiosis (S) only, as shown in Table 2. Distinct letters on boxplots indicate significant differences (P < 0.05) among symbioses based on post-hoc multiple comparisons of means. *P < 0.05; **P < 0.01; ***P < 0.001. DW, dry weight.

Fig. 3.

Concentration of Epichloë-derived ergovaline alkaloid in different plant–endophyte symbioses (indicated through host species name) and plant parts. The category ‘above-ground’ is used to aggregate all data from studies that did not define the tissue type, either vegetative or reproductive. Points around the boxplots are independent studies (N = 246). Asterisks denote significant effects of symbioses (S), plant part (P) or their interaction (S × P) as shown in Table 2. For vegetative and reproductive plant parts, distinct letters on boxplots indicate significant differences (P < 0.05) based on post-hoc multiple comparisons of means. *P < 0.05; **P < 0.01; ***P < 0.001. DW, dry weight.

Fig. 4.

Concentration of Epichloë-derived lolitrem B alkaloid in the symbiosis between Lolium perenne and the common strain of the endophyte fungus Epichloë festucae var. lolii. The category ‘above-ground’ is used to aggregate all data from studies that did not define the tissue type, either vegetative or reproductive. Points around the boxplots are independent studies (N = 146). Asterisks denote significant effects of plant part (P) only, as shown in Table 2. Distinct letters on boxplots indicate significant differences (P < 0.05) among plant parts based on post-hoc multiple comparisons of means. *P < 0.05; **P < 0.01; ***P < 0.001. DW, dry weight.