Whitefly aggregation on tomato is mediated by feeding‐induced changes in plant metabolites that influence the behaviour and performance of conspecifics

Su, Qi; Chen, Gong; Mescher, Mark C.; Peng, Zhengke; Xie, Wen; Wang, Shaoli; Wu, Qingjun; Liu, Jie; Li, Chuanren; Wang, Wenkai; Zhang, Youjun

doi:10.1111/1365-2435.13055

Cited by 49 publications

(66 citation statements)

References 70 publications

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“…To investigate whether T. urticae infestation affects the levels of leaf flavonoids, which function as a resistance factor against whiteflies and TYLCV transmission (Su et al, ; Yao et al, ), we compared flavonoids levels in tomato plants with and without T. urticae . The total flavonoid levels did not differ significantly between tomato plants with and without T. urticae ( F 1,14 = 3.389, p = .087; Figure a).…”

Section: Resultsmentioning

confidence: 99%

“…The preparation was incubated overnight in the dark with gentle shaking. The resulting extracts (10 μl) were analysed by LC‐MS using a Thermo LTQ Orbitrap XL mass spectrometer with electrospray ionization source, coupled to a Thermo Accela 1250 liquid chromatography and autosampler (Thermo‐Fisher) as described previously (Su et al, ). Metabolites were detected using electrospray ionization in negative mode including rutin ( m/z 609), chlorogenic acid ( m/z 639), quinic acid ( m/z 681), quercetin‐trisaccharide ( m/z 695), kaempferol‐rhamnoside ( m/z 737), 3‐ O ‐methylmyricetin ( m/z 779), dehydrotomatine ( m/z 1,066) and tomatine ( m/z 1,078).…”

Section: Methodsmentioning

confidence: 99%

“…Metabolites were detected using electrospray ionization in negative mode including rutin ( m/z 609), chlorogenic acid ( m/z 639), quinic acid ( m/z 681), quercetin‐trisaccharide ( m/z 695), kaempferol‐rhamnoside ( m/z 737), 3‐ O ‐methylmyricetin ( m/z 779), dehydrotomatine ( m/z 1,066) and tomatine ( m/z 1,078). Flavonoids, tomatines and acylsugars were quantified as described by Su et al (). Measured levels of defensive metabolites were normalized to the fresh weight of the leaf used for each extraction, and total metabolite levels were calculated as the sum of all individual compounds.…”

Section: Methodsmentioning

confidence: 99%

“…To examine the effect of specific flavonoids on B. tabaci feeding behaviour and TYLCV transmission, flavonoids were applied to tomato plants using the method as described by Su et al (). Briefly, we slightly abraded the first epidermal layers of the stems of T. urticae ‐infested plants, and then applied a 20‐μl solution of 10 μM rutin or quercetin (Sigma‐Aldrich) dissolved in 1% (v/v) ethanol (buffer) to the abraded area.…”

Section: Methodsmentioning

confidence: 99%

“…Second, previous studies have documented that plant flavonoids deter some chewing herbivores (Kang et al, , ; Malone, Barraclough, Lin‐Wang, Stevenson, & Allan, ; Onkokesung et al, ). Furthermore, a recent study showed that B. tabaci infestation changed tomato flavonoid metabolism and thereby enhanced susceptibility to conspecifics and induced conspecific feeders to aggregate on the host plant (Su et al, ). Additionally, they also suggested that flavonoids can deter B. tabaci feeding and reduce its transmission of TYLCV (Yao et al, ); more specifically, high flavonoid levels in tomato deterred B. tabaci probing and salivating, and therefore reduced the transmission of TYLCV.…”

Section: Introductionmentioning

confidence: 99%

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A non‐vector herbivore indirectly increases the transmission of a vector‐borne virus by reducing plant chemical defences

Yang

Yao

et al. 2020

Functional Ecology

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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

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Section: Resultsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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A non‐vector herbivore indirectly increases the transmission of a vector‐borne virus by reducing plant chemical defences

Yang

Yao

et al. 2020

Functional Ecology

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Ecometabolomics of plant–herbivore and plant–fungi interactions: a synthesis study

et al. 2021

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The functional adaptive responses of higher plants to biotic interactions with herbivores and fungi have long been topics of research. One constraint to obtaining a comprehensive understanding of the most general plant responses, however, has been the difficulty of studying all plant functional shifts simultaneously due to analytical limitations. Now this is possible with the advent of metabolomics. Using 151 records from the WEB of SCIENCE database, we have analyzed the development and application of metabolomic profiles to ecological studies in the last two decades. We have used meta-analysis and pathway enrichment analyses to assess the whole set of constitutive and inducible defenses. Constitutive defenses against herbivores were mainly based on a significant high level of the metabolism of several amino acids with parallel increases in the concentrations of flavones (phenolics) and saponins (glycosides). Inducible defenses, though, were mainly based on the increases in concentration of methyl-ketone, pantothenate, and Coenzyme A. Butyrate metabolism and the mitochondrial electron-transport chain were upregulated, in agreement with previous reports that herbivory-activated plant chemical defenses were mainly based on jasmonic acid, salicylic acid, and ethylene-associated pathways. The metabolic responses/acclimations to pathogenic fungi were mainly linked with increases in aspartate and pyruvate metabolism, the transfer of acetyl groups within mitochondria, and the upregulation of branched-chain amino acids degradation pathways. These responses/acclimations were accompanied by higher concentrations of the most important groups of secondary metabolites such as phenolics (anthocyanins, flavonoids), quinones, alkaloids, terpenoids, and polyamines and other compounds related to antistress mechanisms such as proline. The leaves of mycorrhized plants accumulated nucleotide sugars, sphingolipids, and methylhistidine. These responses were associated with maintaining the integrity of plant cell membranes under fungal hypha penetration. The responses were accompanied by increases in the concentrations of phenolics, blumenols, and alkaloids and decreases in the concentrations of polyamines, consistent with the mycorrhizal inhibition of polyamines. This summary provides a clear synthesis of the most successful plant strategies selected after millions of years of evolution and will be a very promising tool for the management of crops and ecosystems and for selecting the main lines in breeding studies for future research.

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Species‐specific plant‐mediated effects between herbivores converge at high damage intensity

Wan

Tao

et al. 2022

Ecology

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Plants are often exposed to multiple herbivores and densities of these attackers (or corresponding damage intensities) often fluctuate greatly in the field. Plant-mediated interactions vary among herbivore species and with changing feeding intensity, but little is known about how herbivore identity and density interact to determine plant responses and herbivore fitness. Here, we investigated this question using Triadica sebifera (tallow) and two common and abundant specialist insect herbivores, Bikasha collaris (flea beetle) and Heterapoderopsis bicallosicollis (weevil). By manipulating densities of leaffeeding adults of these two herbivore species, we tested how variations in the intensity of leaf damage caused by flea beetle or weevil adults affected the performance of root-feeding flea beetle larvae and evaluated the potential of induced tallow root traits to predict flea beetle larval performance. We found that weevil adults consistently decreased the survival of flea beetle larvae with increasing leaf damage intensities. In contrast, conspecific flea beetle adults increased their larval survival at low damage then decreased larval survival at high damage, resulting in a unimodal pattern. Chemical analyses showed that increasing leaf damage from weevil adults linearly decreased root carbohydrates and increased root tannin, whereas flea beetle adults had opposite effects as weevil adults at low damage and similar effects as them at high damage. Furthermore, across all feeding treatments, flea beetle larval survival correlated positively with concentrations of carbohydrates and negatively with concentration of tannin, suggesting that root primary and secondary metabolism might underlie the observed effects on flea beetle larvae. Our study demonstrates that herbivore identity and density interact to determine systemic plant responses and plant-mediated effects on herbivores. In particular, effects are species-specific at low densities, but converge at high densities. These findings emphasize the importance of considering herbivore identity and density simultaneously when investigating factors driving plant-mediated interactions

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Whitefly aggregation on tomato is mediated by feeding‐induced changes in plant metabolites that influence the behaviour and performance of conspecifics

Cited by 49 publications

References 70 publications

A non‐vector herbivore indirectly increases the transmission of a vector‐borne virus by reducing plant chemical defences

A non‐vector herbivore indirectly increases the transmission of a vector‐borne virus by reducing plant chemical defences

Ecometabolomics of plant–herbivore and plant–fungi interactions: a synthesis study

Species‐specific plant‐mediated effects between herbivores converge at high damage intensity

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