Exploring the interactions between host plants, herbivores, and natural enemies is an important experimental approach for enhancing biological control. Induced plant defense responses following infestation by herbivores enable plants to minimize damage. Zoophytophagous predators induce plant defense responses through feeding. Since the zoophytophagous bug Orius sauteri lays eggs into plant tissues, we hypothesised that its oviposition behaviour may also induce plant defense responses with a negative impact on subsequent herbivore attacks. Pre-inoculation of O. sauteri females on tomato plants significantly reduced the fitness, reproduction, and choice preference of Frankliniella occidentalis compared to the control plants in indoor micro-environments and in the field, whereas this tendency was weaker in males. Next, a transcriptome analysis showed that the MAPK signalling pathway, the plant hormone signal transduction and plant-pathogen interaction of defense-related pathways were significantly enriched in plants inoculated with O. sauteri females compared to untreated plants. We showed that three key genes of the JA pathway, allene oxide synthase (AOS), jasmonate ZIM-domain 2 (JAZ2), and proteinase inhibitor 1 (PI-1), were upregulated. This is evidence of plant defense activation, the likely mechanism by which O. sauteri pre-inoculation (through feeding and oviposition activities) reduced F. occidentalis fitness in the laboratory and population densities by almost three times in a greenhouse experiment. This mechanism could be promoted in IPM strategies through the early introduction of zoophytophagous biocontrol agents activating crop plant defenses to enhance biological pest control.
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