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

Abstract

BACKGROUNDThe 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).RESULTSBy 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.CONCLUSIONOur 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.

Efficiency of Citrus limon L. Ripe Peel Extract In The Control of Raoiella indica (HIRST, 1924) (Prostigmata: Tenuipalpidae)

“…The flavonoids have important roles in the plant metabolism, and can also act as defense substances against pests and pathogens attacks (STEC et al, 2021). Upon entering the arthropods' organism, it can cause biochemical interferences, affect their behavior, reduce the resistance, damage metabolic and physiological processes, such as growing, development, reproduction and oviposition, and lead to death by acute toxicity, feeding deterrence, reducing the nutrient absorption or corrupting metabolic pathways (GAUTAM et al, 2023;YANG et al, 2023;NGATSI et al, 2024;VOLF et al, 2024).…”

1-nonene plays an important role in the response of maize-aphid-ladybird tritrophic interactions to nitrogen

“…Since evidence for an active role of herbivore-damaged plants in recruiting natural enemies of herbivores was first reported, an increasing number of different species of plants have been found to attract a range of herbivore enemies after an herbivore attack, including insect predators, parasitoids, predatory mites, nematodes, and birds ( Clavijo et al., 2012 ; Meijer et al., 2023 ). Thus, tritrophic interactions are being increasingly discussed as an environmentally friendly crop protection strategy ( Heil, 2008 ; Yang et al., 2023 ).…”

Comparative Transcriptomic and Metabolomic Analyses of Differences in Trunk Spiral Grain in Pinus yunnanensis

“…Secondary metabolites are a class of compounds produced by organisms during growth and development and are closely related to their physiological functions and adaptations to the environment [28][29][30]. There is a close relationship between secondary metabolites and phenotype, and the type and content of secondary metabolites can directly affect the phenotypic characteristics of organisms [31]. For example, the secondary metabolites of some plants have biological activities such as antibacterial and antipest activities, which can protect plants from the external environment, thus affecting the growth and morphological characteristics of plants [31,32].…”

“…There is a close relationship between secondary metabolites and phenotype, and the type and content of secondary metabolites can directly affect the phenotypic characteristics of organisms [31]. For example, the secondary metabolites of some plants have biological activities such as antibacterial and antipest activities, which can protect plants from the external environment, thus affecting the growth and morphological characteristics of plants [31,32]. In addition, secondary metabolites can also affect the external manifestations of organisms, such as color [33], taste [34], and aroma [35], which, in turn, affect the reproduction [31] and adaptability [30] of organisms.…”

“…For example, the secondary metabolites of some plants have biological activities such as antibacterial and antipest activities, which can protect plants from the external environment, thus affecting the growth and morphological characteristics of plants [31,32]. In addition, secondary metabolites can also affect the external manifestations of organisms, such as color [33], taste [34], and aroma [35], which, in turn, affect the reproduction [31] and adaptability [30] of organisms. The production and regulation of secondary metabolites are closely related to the phenotypic plasticity of organisms [36].…”