Flavonoid production in tomato mediates both direct and indirect plant defences against whiteflies in tritrophic interactions

The role of plant flavonoids in direct defences against chewing and sap-sucking herbivorous insects has been extensively characterized. However, little is known about flavonoid-mediated tritrophic interactions between plants, herbivorous insects and natural enemies. In this study, we investigated how flavonoids modulate plant-insect interactions in a tritrophic system involving near-isogenic lines (NILs) of cultivated tomato (Solanum lycopersicum) with high (line NIL-purple hypocotyl [PH]) and low (line NIL-green hypocotyl [GH]) flavonoid levels, with a generalist herbivore whitefly (Bemisia tabaci) and its predatory bug (Orius sauteri).By contrasting levels of tomato flavonoids (direct defence) while manipulating the presence of predators (indirect defence), we found that high production of flavonoids in tomato was associated with a higher inducibility of direct defences and a stronger plant resistance to whitefly infestation and stimulated the emissions of induced volatile organic compounds, thereby increasing the attractiveness of B. tabaci-infested plants to the predator O. sauteri. Furthermore, suppression of B. tabaci population growth and enhancement of plant growth were mediated directly by the high production of flavonoids and indirectly by the attraction of O. sauteri, and the combined effects were larger than each effect individually.Our results show that high flavonoid production in tomato enhances herbivore-induced direct and indirect defences to better defend against herbivores in tritrophic interactions. Thus, the development of transgenic plants may present an opportunity to utilize the beneficial role of flavonoids in integrated pest management, while simultaneously maintaining or improving resistance against other pests and pathogens. © 2023 Society of Chemical Industry.