Plant-mediated interactions between the entomopathogenic fungus Beauveria bassiana, insect herbivores and a plant pathogen

Abstract

The entomopathogenic fungus Beauveria bassiana can adopt an endophytic lifestyle by colonising a wide array of plant species. Several studies have reported enhanced resistance against insects and plant pathogens from colonised plants. However, little is known about the molecular and physiological mechanisms that govern such interactions. Elucidating the responses of the plant is therefore needed and will help to better understand this recently discovered aspect in the ecology of entomopathogens. The B. bassiana strains FRh2 and BG11 were used in this study. Their antagonistic effects, as endophytes, on the necrotic fungus Sclerotinia sclerotiorum and the two herbivore species Myzus persicae and Plutella xylostella were assessed. Treatment of Arabidopsis thaliana roots with B. bassiana FRh2 and BG11 significantly decreased leaf lesion size caused by S. sclerotiorum but did not affect M. persicae population growth and P. xylostella body mass. Genome expression analysis of A. thaliana leaves 15 days post infestation provided evidence for transcriptional reprogramming and induction of plant defence pathways following colonisation by both B. bassiana strains. The transcriptional responses aligned with reports on A. thaliana interaction with other plant growth promoting fungi such as the known root endophytes Trichoderma spp. and Piriformospora indica. The results also showed that B. bassiana strains FRh2 and BG11 colonisation evoked microbe-associated molecular pattern triggered immunity and the induction of several jasmonic (JA) and salicylic acid (SA) signalling pathway genes. Furthermore, systemic colonisation of plant tissue by FRh2 and BG11 resulted in the induction of genes involved in the biosynthesis of the antimicrobial phytoalexin camalexin and genes encoding multiple reactive oxygen species scavengers such as peroxidases and glutathione transferases. However, JA levels measured in FRh2 and BG11 colonised plants were only induced by P. xylostella caterpillar feeding but were not influenced by the presence of the fungus. Neither caterpillar feeding nor B. bassiana presence had an effect on endogenous SA levels. Also, B. bassiana colonisation by either strain did not result in major changes in leaf glucosinolate profiles, although a lower content of total aliphatic glucosinolates was recorded in FRh2 colonised Arabidopsis only. Based on this, it can be speculated that camalexin-induction by B. bassiana, and possibly priming of SA or JA mediated defences, could have resulted in enhanced resistance against S. sclerotiorum. However, since B. bassiana colonised both roots and shoots, direct effects on the pathogenic fungus cannot be ruled out entirely. Further investigations are required to determine the mechanisms underlying the protective effects of B. bassiana against S. sclerotiorum infection. This is one of the first studies to assess the metabolic and transcriptomic responses of a plant colonised by the entomopathogen B. bassiana and showed induction in the expression of host defence-related genes.