Foliar phosphorus concentration modulates the defensive mutualism of an endophytic fungus in a perennial host grass

Grasses hosting Epichloë endophytes are protected against herbivores due
to the production of various fungal alkaloids. Previous research has found
that high foliar phosphorus concentrations reduce the level of the
alkaloid ergovaline, thereby reducing the endophyte-mediated herbivore
resistance. Yet, the impact of phosphorus on ergovaline biosynthesis
versus its influence on endophyte growth and synthesis of other fungal
alkaloids remains unresolved. Our objective was to elucidate these
relationships. We grew endophyte-symbiotic and non-symbiotic
Festuca arundinacea plants and fertilized them with different doses of
phosphorus. Later, half of the plants from each treatment were challenged
with larvae of the generalist chewing insect Spodoptera frugiperda. We
assessed the relationships between foliar phosphorus levels, fungal
mycelium, and alkaloid concentrations, as well as their impacts on larvae
performance, herbivore-caused damage, and plant biomass. Endophyte
mycelial biomass in plant tissue was found to be independent of foliar
phosphorus concentration. The alkaloids lolines and peramine showed a
linear relationship with mycelial biomass but no correlation with foliar
phosphorus. Surprisingly, high ergovaline concentrations were positively
associated with an interaction between endophyte mycelial biomass and
foliar phosphorus concentration. Although herbivory increased loline
concentration, only high concentrations of ergovaline and peramine were
related to reduced S. frugiperda larvae weight gain. However, endophyte
presence did not reduce herbivory damage to plants. Contrary to
expectation, we did not find a negative but a positive association between
concentrations of foliar phosphorus and ergovaline alkaloid, through its
interaction with endophyte mycelial biomass. Alternatively, our findings
suggest that phosphorus plays a crucial role in modulating the
Epichloë-mediated defensive mutualism, primarily through its effects on
ergovaline rather than on endophyte concentration or production of other
alkaloids.