Host plants benefit from non-predatory effects of zoophytophagous predators against herbivores

Abstract

Zoophytophagous predators can induce plant defence responses through phytophagous feeding. Since the zoophytophagous bug Orius sauteri lays eggs into plant tissues, we hypothesised that its oviposition behaviour may also induce plant defence responses with a negative impact on subsequent herbivore attacks. Pre-inoculation of O. sauteri females on tomato plants significantly reduced the fitness and reproduction of Frankliniella occidentalis, which also preferred the non-inoculated plants in indoor micro-environments. In the field, O. sauteri pre-inoculation also caused reduced population growth of F. occidentalis. All these tendencies were weaker with male compared to female O. sauteri pre-inoculation. Next, a transcriptome analysis showed that the MAPK signalling pathway, the plant hormone signal transduction and plant-pathogen interaction of defence-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 defence 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 defences to enhance biological pest control.