Invisible but consequential: Root endophytic fungi have variable effects on belowground plant-insect interactions

Abstract

Endophytic fungi are ubiquitous in nature and can play important roles in regulating plant- herbivore interactions. While some aboveground obligate symbionts are considered defensive mutualists of host plants, the importance of root endophytes in plant defense, especially against root-feeding insects, remains unclear. This study aimed to investigate the effects of root fungal endophytes on plant resistance against belowground herbivores and the recovery of host plants from damage. We grew the common grass Festuca arundinacea (tall fescue) semi-Aeroponically in the laboratory and inoculated roots with one of five fungal endophytes isolated from field-collected tall fescue or meadow soil. Endophyte-inoculated and uninoculated control plants were subjected to feeding by larvae of the generalist root herbivore Rhizotrogus majalis (European chafer). Herbivory intensity was quantified after eight days, and regrowth of roots and shoots following root herbivory and mechanical shoot damage was measured thereafter for each treatment. Fungal identifications by DNA sequence analysis were conducted after completion of the herbivory experiments and revealed that the five endophytes included the decomposer fungi Trametes versicolor and Mortierella alpina, the entomopathogenic fungi Isaria fumosorosea and Beauveria bassiana, and a potential plant pathogen/entomopathogen Fusarium cf. equiseti. The effects of these root endophytes on plant defense against root-feeding insects were species-specific. While four endophytes had few effects on plant resistance, endophytic B. bassiana significantly reduced herbivore damage to roots. In comparison, plant tolerance to damage was impaired after colonization by all endophyte species except T. versicolor and M. alpina. The contrasting effects of endophytes on plant resistance and plant tolerance suggest that research solely evaluating plant resistance is likely to overestimate the benefits conferred by endophytes without accounting for potential negative effects on plant tolerance. We propose a conceptual framework to include both plant resistance and tolerance as two dimensions of a defensive strategy and show that plant associations with different root endophytes may shift the relative importance of resistance and tolerance for plant defense.