Invisible but consequential: root endophytic fungi have variable effects on belowground plant–insect interactions

Abstract

Abstract. Endophytic fungi are ubiquitous in nature and can play important roles in regulating plantherbivore 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.

Strategies for Enhanced Crop Resistance to Insect Pests

“…fungal endophytes and mycorrhizal fungi, can influence herbivory (30,55,73,99) and that the plant range of some insects is shaped by their microbiome (21). Although most research to date has focused almost exclusively on the fundamentals of microbial impacts on plant-insect interactions, there is a growing appreciation of opportunities for crop protection.…”

The Beneficial Endophytic Fungus Fusariumsolani Strain K Alters Tomato Responses Against Spider Mites to the Benefit of the Plant

“…Nevertheless, a number of diverse endophytic fungi are known to also inhabit roots, forming variable associations with the plants, ranging from parasitic to mutualistic, without, however, causing apparent disease symptoms in plants ( Wilson, 1995 ; Schulz and Boyle, 2005 ; Hartley and Gange, 2009 ; Rodriguez et al, 2009 ). In contrast to AMF, the ecological roles of the most common endophytic fungi, especially those that are horizontally transmitted via spores (e.g., Ascomycetes), currently remain elusive although generally believed to also play an important role in plant protection against herbivores ( Jaber and Vidal, 2009 ; Rodriguez et al, 2009 ; Gan et al, 2017 ). Indeed, certain root endophytic fungi have been shown to increase the expression of defense-related genes and the production of secondary metabolites that may be relevant to plant defense ( Pieterse et al, 2014 ).…”

“…In addition, a few studies involving endophytic fungi have reported negative effects on above ground herbivores thus enhancing their potent role in plant resistance to biotic stressors ( Jallow et al, 2004 ; Jaber and Vidal, 2009 , 2010 ; Muvea et al, 2014 ; Coppola et al, 2017 ; Contreras-Cornejo et al, 2018 ). Nevertheless, our understanding of endophytic fungi – plant – herbivore interactions is still at its infancy thus calling for more empirical studies on the significance of horizontally transmitted endophytes in plant–herbivore interactions ( Gan et al, 2017 ).…”

Endophytic Bacterial Microbiome Diversity in Early Developmental Stage Plant Tissues of Wheat Varieties

“…It is relatively unusual for a plant to be colonized by only one type of endophyte. The high number of species and high amount of microbial biomass in small populations suggest frequent multitrophic interactions between bacteria, micro-and macroscopic fungi, microfauna, plants and the environment [8][9][10].…”