No abstract

Tomato yellow leaf curl virus (TYLCV), a begomovirus (genus Begomovirus) is the causal agent of tomato yellow leaf curl disease (TYLCD), which causes severe damage to tomato (Solanum lycopersicum) crops throughout tropical and subtropical regions of the world. TYLCV is transmitted by the whitefly Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae) in a circulative and persistent manner. Our previous studies showed that tomato flavonoids deter B. tabaci oviposition, but the effects of tomato flavonoids on the settling and feeding behavior of B. tabaci and on its transmission of TYLCV are unknown. Using two near-isogenic tomato lines that differ greatly in flavonoid levels, we found that high flavonoid production in tomato deterred the landing and settling of B. tabaci. Moreover, electrical penetration graph studies indicated that high flavonoid levels in tomato reduced B. tabaci probing and phloem-feeding efficiency. As a consequence, high flavonoid levels in tomato reduced the primary and secondary spread of TYLCV. The results indicate that tomato flavonoids provide antixenosis resistance against B. tabaci and that the breeding of such resistance in new varieties could enhance TYLCD management.

1. Vectors and viruses exist in communities consisting of many interacting species.Although the cascading effects of predators or parasitoids on disease spread via direct effects on vectors have been investigated, little is known about the effects of other free-living species in communities on the transmission of vector-borne viruses via indirect (host-plant mediated) effects on vectors.2. In the present study, we used a food web consisting of tomato plants Solanum lycopersicum, two tomato herbivores (the vector whitefly, Bemisia tabaci, and the non-vector two-spotted spider mite, Tetranychus urticae) and a whitefly-vectored plant virus (Tomato yellow leaf curl virus, TYLCV) to study how T. urticae may affect TYLCV transmission by B. tabaci via host-plant mediated effects on B. tabaci.3. We found that T. urticae infestation promoted B. tabaci feeding, thereby increasing TYLCV transmission to tomato plants. These increases were associated with T. urticae-induced reductions in two flavonoids (rutin and quercetin trisaccharide) of tomato plants. Elevation of rutin and quercetin trisaccharide levels in T. urticae-infested plants via exogenous stem applications reduced B. tabaci feeding and TYLCV transmission. Therefore, suppression of these flavonoids by T. urticae infestation was the most likely explanation for the observed changes in B. tabaci feeding behaviour and TYLCV transmission. 4. Our results show that by reducing flavonoids in tomato plants, a non-vector herbivore can indirectly increase the transmission of a vector-borne plant virus. These findings indicate that species that are far removed from the direct vector-virus interactions can indirectly affect vector-borne virus transmission by altering the chemical defences of the shared host plant. K E Y W O R D S Bemisia tabaci, community ecology, disease ecology, flavonoids, herbivore-plant-virus interactions, Solanum lycopersicum, Tetranychus urticae

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.