In the tripartite combination Botrytis cinerea–Arabidopsis–Eurydema oleracea, the fungal pathogen alters the plant–insect interaction via jasmonic acid signalling activation and inducible plant-emitted volatiles

Abstract

In ecosystems, plants are continuously challenged by combined stress conditions more than by a single biotic or abiotic factor. Consequently, in recent years studies on plant relationships with multiple stresses have aroused increasing interest. Here, the impact of inoculation with fungal pathogens with different lifestyles on Arabidopsis plants response to the following infestation with the invasive crop pest Eurydema oleracea was investigated. In particular, as fungal pathogens the necrotroph Botrytis cinerea and the biotroph Golovinomyces orontii were used. Plants exposed to B. cinerea, but not to G. orontii, showed reduced herbivore feeding damage. This difference was associated to different hormonal pathways triggered by the pathogens: G. orontii only induced the salicylate-mediated pathway, while B. cinerea stimulated also the jasmonate-dependent signalling, which persisted for a long time providing a long-term defence to further herbivore attack. In particular, the lower susceptibility of B. cinerea-infected Arabidopsis plants to E. oleracea was related to the stimulation of the JA-induced pathway on the production of plant volatile compounds, since treatment with VOCs emitted by B. cinerea inoculated plants inhibited both insect plant choice and feeding damage. These results indicate that necrotrophic plant pathogenic fungi modulate host volatile emission, thus affecting plant response to subsequent insect, thereby increasing the knowledge on tripartite plant–microbe–insect interactions in nature.

Increasing the activities of protective enzymes is an important strategy to improve resistance in cucumber to powdery mildew disease and melon aphid under different infection/infestation patterns

“…Previous studies have shown that one premise for pathogens and insects to choose cooperative or non-cooperative relationships is the order in which they infect host plants ( Meng, 2013 ). When a pathogen first infects a plant, it will induce the plant to produce volatile substances to avoid insect attack ( Ederli et al, 2021 ), and synergistic interactions between pathogens and insects have been utilized as a classical approach to the biological control of weeds ( Willsey et al, 2017 ). However, when insects first attack, they often do not adversely affect the pathogens that subsequently infect, and make the host even more conducive to infection by pathogens ( Li et al, 2021 ).…”

Metabolic and Transcriptomic Profiling of Lilium Leaves Infected With Botrytis elliptica Reveals Different Stages of Plant Defense Mechanisms

“…Moreover, as reported in the interactions between other hosts and Botrytis spp. (e.g., Arabidopsis – B. cinerea and Arabidopsis – Alternaria brassicicola ), the SA and JA signaling pathways play a crucial role in the response of “Sorbonne” to fungal infection (Zheng et al, 2006 ; Ederli et al, 2015 , 2021 ; Liao et al, 2020 ). Besides, the BR-related genes were significantly up-regulated during across all infection stages in our results.…”

Effect of zinc imbalance and salicylic acid co‐supply on Arabidopsis response to fungal pathogens with different lifestyles

“…The PCR programme for PDF 1.2 was as reported in Ederli et al . ( 2021 ) with slight modifications. Briefly, it consisted of 94 °C for 1 min 15 s, 32 cycles of 5 s at 94 °C, 20 s at 57.5 °C and 45 s at 72 °C, followed by 6 min at 72 °C.…”