Growth-promoting rhizobacteria amend the defense of strawberry plants against sequentially attacking herbivores

Plant defense systems such as induced resistance (IR; induced by herbivores) and induced systemic resistance (ISR; induced by beneficial rhizobacteria) are modulated by the same signaling pathways within plants and hence interact. ISR allows enhanced protection of aboveground plant parts against herbivores before IR induction. Both ISR and IR are systemic and may involve the production of toxic, antifeedant and/or repellent compounds, and/or reduce nutrient availability, which may in consequence affect plant usability and palatability for later arriving herbivores. The combined effects of ISR and IR on different herbivores sharing the same plant and plant performance have been rarely addressed. Here, we assessed the effects of three plant-growth-promoting rhizobacteria (PGPR), Azotobacter chroococcum, Azospirillum brasilense and Pseudomonas brassicacearum, on the defense response and physiology of strawberry plants upon sequential attack by two herbivores with different feeding modes, two-spotted spider mites Tetranychus urticae and cotton aphids Aphis gossypii. Attack of strawberry plants by spider mites and aphids adversely affected the abundance of the later arriving herbivore, mediated by the host plants defense system. First-attacking spider mites exerted much stronger adverse effects on later attacking aphids than first-attacking aphids on later attacking spider mites. In absence of PGPR inoculation, the herbivores, especially first-attacking spider mites, severely impaired host plant physiology and productivity. PGPR inoculation primed the plants defense system to attack by spider mites and aphids, allowing the plants to produce more secondary metabolites such as phenols. In consequence, the abundances of both herbivores were lower on PGPR-inoculated plants compared to chemically fertilized and control plants. Overall, our study suggests that PGPR inoculation ameliorates the plant damage caused by sequentially attacking herbivores. Additionally, the PGPRs improve the physiology and productivity, and favorably balance the nutritional state, of strawberry plants.