Psoralens in senescing leaves ofRuta graveolens

Concentrations of three furanocoumarins, psoralen, xanthotoxin, and bergapten, were measured on the surface and within mature whole leaves of two groups ofRuta graveolens L. late autumn plants, 2 and 6 years old, which contained green, yellow, and dry yellow leaves. Upper green leaves contained higher concentrations of these coumarins than lower green leaves, green leaves contained several times as much as yellow leaves, and dry leaves contained even smaller amounts than yellow ones. The dry yellow leaves contained only a very small percentage of furanocoumarins on the surface, suggesting that extrusion to the surface of yellow leaves was slower or had stopped, while loss from the surface continued. The loss of psoralen was the most dramatic in and on the dry leaves. Bergapten's ratio to the other cournarins increased during senescence. Xanthotoxin was always the predominant furanocoumarin in this species.     

Seasonal changes of furanocoumarin concentrations in leaves ofHeracleum lanatum

Concentrations of three dermatitis-inducing furanocoumarins— xanthotoxin, bergapten and psoralen—were measured in whole leaves ofHeracleum lanatum and in extracts of the leaf surface over an entire vegetative season. The concentrations of surface furanocoumarins, localized by extraction involving brief dipping in almost-boiling water followed by HPLC quantitative analysis, increased until the middle of May and decreased until maturity. The concentration on autumn leaves (new growth) was 20–100 times as high as the ones in May, or those of similar size in April. Furanocoumarin concentrations in the whole leaf at different stages of leaf development varied, being the highest April 25, then decreasing sharply with rapid leaf enlargement. Again, in the small autumn leaves the coumarin concentration was two to three times that in April. Seasonal changes in surface furanocoumarins may be important in that these compounds are postulated to form the first defense barrier of the plant.     

Dermatitis-inducing furanocoumarins on leaf surfaces of eight species of Rutaceous and Umbelliferous plants

Eight species of Rutaceae or Umbelliferae, known to cause or suspected of causing photophytodermatitis, had the linear furanocoumarins psoralen, bergapten, and xanthotoxin on their leaf surfaces, in concentrations varying from 0.014 to 1800 /gmg/g fresh weight, equivalent to 0.17–56% of the total leaf concentration. The higher percentage generally observed for spring leaves compared to autumn leaves suggests a higher rate of transfer of these furanocoumarins to the surface in the younger leaves. Among the plants studied,Ruta graveolens had the highest surface concentrations of all three furanocoumarins. The relatively high effectiveness in causing dermatitis of some species with low surface concentrations may be explained by a more effective mechanism of transfer of the furanocoumarins to the skin. A role in the defense of the plant is suggested by their accumulation on the plant surface.A paper based on the work reported here was presented at the Groupe Polyphénols conference, Brock University, St. Catharines, Ontario, Canada, August 19–19, 1988.     

Toxicity of linear furanocoumarins toSpodoptera exigua: Evidence for antagonistic interactions

The linear furanocoumarins psoralen, bergapten, and xanthotoxin were tested for toxicity to the beet armywormSpodoptera exigua (Hübner) under short ultraviolet (UVB) radiation. Increased dietary concentrations of each furanocoumarin significantly decreased insect larval weight, extended generation time, and induced higher mortality. Xanthotoxin was the most toxic, followed by psoralen and bergapten. Combining psoralen with bergapten, xanthotoxin, or both resulted in significantly antagonistic effects on insect mortality. The combination of bergapten and xanthotoxin, however, produced additive effects. The implications of these observations forS. exigua resistance in the wild plant accession ofApium prostratum and the enigma the findings represent for plant-insect relationships are discussed.     

Influence of low-intensity ultraviolet radiation on extrusion of furanocoumarins to the leaf surface

Exposure ofRuta graveolens leaves to low intensity 366-nm radiation led to a ca. 20% increase in concentrations of the furanocoumarins psoralen, xanthotoxin and bergapten, as compared to leaves kept in darkness. Both direct and, even more, scattered UV radiation produced increases in total concentrations. Changes in the concentrations of individual coumarins were generally parallel. Extrusion to the surface was increased, especially in lower, older leaves exposed to the scattered radiation, where it exceeded the control by factors of eight or nine. It is suggested that this response could enhance shielding of leaves against penetration of UV into the cells and that irradiation, by exciting the furanocoumarins, could augment protection against potential microbial invaders.     

Evaluation of Synergism in the Feeding Deterrence of Some Furanocoumarins on Spodoptera littoralis

The phagodepression activity of five furanocoumarins (FC), bergapten, xanthotoxin, psoralen, imperatorin, and angelicin, has been studied against larvae of Egyptian cotton leafworm Spodoptera littoralis (Boisduval) (Lepidoptera: Noctuidae) using a leaf-disk choice bioassay. The dose range used was 0–10 g/cm² for linear furocoumarins and 0–30 g/cm² for angelicin, the angular furanocoumarin. Dose–feeding deterrency activity correlations were governed by various sigmoidal functions, except in the case of imperatorin and bergapten, which had dose–response curves showing irregular traces with two maxima. All five FCs induced various degrees of phagodepression in S. littoralis; at 3 g/cm², the relative feeding deterrence was bergapten = xanthotoxin > psoralen = imperatorin = angelicin. Structure–activity correlations indicated that a methoxy group on C-5 or C-8 enhanced the activity. Comparison of experimental feeding deterrence of binary mixtures of imperatorin with xanthotoxin, bergapten, or psoralen at various relative concentrations with the calculated additive activity of each combination indicated that a proportion of 40% or more of imperatorin may exert a greater antifeedant effect on S. littoralis than the sum of individual compounds. The effect of angelicin also was examined in combination with psoralen, both of which are present in Psoralea plants. Their mixtures yielded a clear synergistic effect in the 20–80% angelicin range (coactivity coefficient = 124–133). By contrast, the effect of angelicin on xanthotoxin was only additive. In the dose–response curves of imperatorin/bergapten combinations, synergism was found at >60% imperatorin relative concentration and 1 g/cm², whereas lower proportions led to antagonism. The threshold between the two opposing effects was found to depend on the total FC concentration employed. Some natural systems contain FCs in the range of synergistic proportions recorded here and, thus, may have been produced by the host to increase its defensive effect at a lower metabolic cost.     

Impact of atmospheric pollution on linear furanocoumarin content in celery

In a series of laboratory studies, a single 4-hr acidic fog at pH levels associated with commercial celery (Apium graveolens L.) production near major population centers in California was found to stimulate development of psoralen, bergapten, xanthotoxin, and isopimpinellin within 24 hr and for at least 120 hr after exposure. At 120 hr posttreatment, the concentrations of phototoxin furanocoumarins (psoralen + bergapten + xanthotoxin) increased 540% in the leaves (to 135 g/g fresh weight) and 440% in the petioles (to 55.56 g/g fresh weight) of celery exposed to a pH 2.0 fog as compared to plants exposed to control fogs (pH 6.3–6.5). Concentrations of these compounds in test plants were 7.5 times higher than the amount known to produce contact dermatitis. The nonphototoxic isopimpinellin increased more than threefold in the leaves (to 39.23 g/g fresh weight, 120 hr) and petioles (to 25.88/gmg/g fresh weight) as compared to control plants. In contrast, a single ozone fumigation at 0.20 ppm for 2 hr generally reduced concentrations of phototoxin furanocoumarin in leaves of celery within 24 hr (ozone-treated plants = 37.9, controls = 69.5 g/g fresh weight), but levels of these chemicals in leaves of ozone-fumigated plants increased rapidly and concentrations were not significantly different at 120 hr. Isopimpinellin concentrations in foliage followed a similar trend (at 24 hr, control = 25.11, ozone treated = 10.96/gmg/g fresh weight, no difference at 120 h). In petioles, none of the linear furanocoumarin levels differed significantly at 120 hr posttreatment.     

Defense of parsnip webworm against phototoxic furanocoumarins: Role of antioxidant enzymes

The parsnip webworm,Depressaria pastinacella (Lepidoptera: Oecophoridae), feeds on plants rich in furanocoumarins, phototoxic allomones. Final-instar larvae possess high levels of activities of antioxidant enzymes (Superoxide dismutase, catalase, glutathione reductase), which detoxify oxygen radicals generated from the furanocoumarins of their host plants. When added to an artificial diet, three linear furanocoumarins (xanthotoxin, bergapten, imperatorin) do not increase levels of the antioxidant enzymes. However, on diets containing both xanthotoxin and piperonyl butoxide, a cytochrome P-450 inhibitor, food utilization indices of the insect are reduced and superoxide dismutase activity is enhanced. These data suggest that cytochrome P-450s act as a primary detoxification system of ingested furanocoumarin, and antioxidant enzymes as a backup system to detoxify oxygen radicals generated by unmetabolized furanocoumarins.     

Allelochemicals fromPilocarpus goudotianus leaves

The effect on germination, shoot, and root growth by bergapten, xanthotoxin, imperatorin, xanthyletin, xanthoxyletin, luvangetin, donatin and alloxanthoxyletol fromPilocarpus goudotianus leaves, onLactuca sativa var. nigra seedlings has been evaluated. A structure-activity correlation is discussed based on the bioassay results. Furanocoumarins appear to be the most active compounds in comparison with pyrano- and simple coumarins. The presence of an oxygenated function at C-8 decreases the germination effect in furano- and pyranocoumarins, while C-5 substituents do not cause significant changes on the activity.Part 2 in the series:Natural Product Models as Allelochemicals. For Part 1 see: Macíaset al. (1992).     

Systemic Induction of Terpenoid Aldehydes in Cotton Pigment Glands by Feeding of Larval Spodoptera exigua

Pigment glands in cotton contain terpenoid aldehydes that are toxic and deterrent to feeding of several generalist lepidopteran insects. We hypothesized that previously observed systemically induced feeding deterrence may be associated with pigment glands. We conducted experiments to determine the dynamics and chemical nature of inducible feeding deterrents in leaves of cotton, Gossypium hirsutum L, to larvae of the beet armyworm, Spodoptera exigua. Production and/or filling of pigment glands was influenced by physiological age of Deltapine 90 cotton plants. In undamaged plants, successively formed leaves contained more pigment glands, up to the seventh or eighth true-leaf developmental stage. Feeding choice tests conducted one or seven days after initial feeding damage revealed that third instars of S. exigua consumed more of the two youngest leaves from control cotton plants than from plants whose two oldest leaves had been fed on previously for 24 hr by S. exigua. The preference for leaves from control plants was significant one day after initial damage and highly significant seven days after damage. Consumption of mature foliage (leaf immediately above initially damaged leaves) from control plants and damaged plants did not differ. More pigment glands were counted on the youngest leaf of damaged plants than on the youngest leaf of control plants one day after initial damage. HPLC analysis revealed greater amounts of hemigossypolone, heliocides 1 and 2 (H₁ and H₂), and total terpenoid aldehydes per gland in young foliage of damaged plants than control plants one day after initial injury. By seven days after initial injury, greater quantities of hemigossypolone and all heliocides except H₄ were detected in young foliage from damaged plants compared to control plants. Concentrations of H₁ per gland in young leaves from damaged plants increased the most of all terpenoid aldehydes measured (3.4× the amount found in leaves from control plants). Mature leaves from damaged plants did not contain more terpenoid aldehydes than mature leaves from control plants. We suggest that systemically induced feeding deterrence to S. exigua in young leaves of glanded cotton was due to increased amounts of terpenoid aldehydes in pigment glands.     

Analysis,isolation and insecticidal activity of linear furanocoumarins and other coumarin derivatives fromPeucedanum (Apiaceae: Apioideae)

Peucedanum arenarium Waldst. & Kit.,P. austriacum (Jacq.) Koch,P. coriaceum Reichenb.,P. longifolium Waldst. & Kit,P. officinale L.,P. oreoselinum (L.) Moench,P. ostruthium L., andP. palustre (L.) Moench accumulate different structural types of coumarins including simple coumarins, linear furanocoumarins, linear dihydropyranocoumarins, angular dihydrofuranocoumarins and angular dihydropyranocoumarins. Linear furanocoumarins, known for various biological activities, include some well-known antifeedants, such as bergapten, isopimpinellin, and xanthotoxin. The aim of this investigation was to screen the diverse coumarins fromPeucedanum for insecticidal activity. LC was used to analyze and isolate coumarins for the bioassays. A growth inhibition bioassay with 17 derivatives, comprising all structural types fromPeucedanum, carried out withSpodoptera littoralis (Boisduval) (Lepidoptera: Noctuidae) as test organism, indicated the majority of the linear furanocoumarins and the angular dihydrofuranocoumarin athamantin as active compounds. Oxygenation of the prenyl residue of linear furanocoumarins decreased activity. Further formation of an ester with angelic acid even resulted in complete inactivity. Five active linear furanocoumarins, bergapten, isopimpinellin, xanthotoxin, isoimperatorin, and imperatorin, and two linear furanocoumarins with a substituted furan ring, peucedanin and 8-methoxypeucedanin, were compared in a dietary utilization bioassay. Relative growth rate (RGR) and relative consumption rate (RCR) divided the tested coumarins in three groups of similar activity. Isopimpinellin and peucedanin slightly decreased RGR and RCR of the treated larvae, and xanthotoxin, isoimperatorin, and 8-methoxypeucedanin heavily decreased RGR and RCR. Bergapten and imperatorin differed by the lowest RGR values and rather high RCR values. The effects caused by these two coumarins indicate specific postingestive toxicity. The results obtained in this study add to the reputation of coumarins to be an effective chemical defense, postulating that chemical diversity is a necessary trait for well-defended plants.     

Systemically Induced Plant Volatiles Emitted at the Time of “Danger”

Feeding by Pieris brassicae caterpillars on the lower leaves of Brussels sprouts (Brassica oleracea var. gemmifera) plants triggers the release of volatiles from upper leaves. The volatiles are attractive for a natural antagonist of the herbivore, the parasitoid Cotesia glomerata. Parasitoids are attracted only if additional damage is inflicted on the systemically induced upper leaves and only after at least three days of herbivore feeding on the lower leaves. Upon termination of caterpillar feeding, the systemic signal is emitted for a maximum of one more day. Systemic induction did not occur at low levels of herbivore infestation. Systemically induced leaves emitted green leaf volatiles, cyclic monoterpenoids, and sesquiterpenes. GC-MS profiles of systemically induced and herbivore-infested leaves did not differ for most compounds, although herbivore infested plants did emit higher amounts of green leaf volatiles. Emission of systemically induced volatiles in Brussels sprouts might function as an induced defense that is activated only when needed, i.e., at the time of caterpillar attack. This way, plants may adopt a flexible management of inducible defensive resources to minimize costs of defense and to maximize fitness in response to unpredictable herbivore attack.     

Interactive Influence of Leaf Age,Light Intensity,and Girdling on Green Ash Foliar Chemistry and Emerald Ash Borer Development

Biotic and abiotic environmental factors affect plant nutritional quality and defensive compounds that confer plant resistance to herbivory. Influence of leaf age, light availability, and girdling on foliar nutrition and defense of green ash (Fraxinus pennsylvanica Marsh) was examined in this study. Longevity of the emerald ash borer, Agrilus planipennis Fairmaire (Coleoptera: Buprestidae), adults reared on green ash foliage subjected to these factors was assayed. Mature leaves generally were more nutritious with greater amino acids and a greater ratio of protein to non-structural carbohydrate (P:C) than young leaves, in particular when trees were grown in shade. On the other hand, mature leaves had lower amounts of trypsin and chymotrypsin inhibitors, and total phenolics compared to young leaves. Lower defense of mature leaves alone, or along with higher nutritional quality may lead to increased survival and longevity of emerald ash borer feeding on mature leaves. Sunlight reduced amino acids and P:C ratio, irrespective of leaf age and girdling, and elevated total protein of young foliage, but not protein of mature leaves. Sunlight also dramatically increased all investigated defensive compounds of young, but not mature leaves. Girdling reduced green ash foliar nutrition, especially, of young leaves grown in shade and of mature leaves grown in sun. However emerald ash borer performance did not differ when fed leaves from trees grown in sun or shade, or from girdled or control trees. One explanation is that emerald ash borer reared on lower nutritional quality food may compensate for nutrient deficiency by increasing its consumption rate. The strong interactions among leaf age, light intensity, and girdling on nutrition and defense highlight the need for caution when interpreting data without considering possible interactions.     

Metabolism and excretion of the furanocoumarin xanthotoxin by parsnip webworm,Depressaria pastinacella

The parsnip webworm,Depressaria pastinacella, feeds on plants containing high concentrations of furanocoumarins. compounds toxic to many organisms. Parsnip webworm larvae were fed radiolabeled xanthotoxin to quantify the detoxification of this furanocoumarin. They metabolized approximately 95% of the ingested xanthotoxin, indicating that metabolic detoxification is important in their tolerance to this allelochemical. Excretion of xanthotoxin and its metabolites was not restricted to the frass but also occurred by means of the silk glands. The silk glands contained half as much of the tritiated compounds as the rest of the body. Because of the feeding habits of this insect, such an excretory pathway may have implications for interactions with predators and pathogens.     

Flower <Emphasis Type="Italic">vs.</Emphasis> Leaf Feeding by <Emphasis Type="Italic">Pieris brassicae</Emphasis>: Glucosinolate-Rich Flower Tissues are Preferred and Sustain Higher Growth Rate

Interactions between butterflies and caterpillars in the genus Pieris and plants in the family Brassicaceae are among the best explored in the field of insect–plant biology. However, we report here for the first time that Pieris brassicae, commonly assumed to be a typical folivore, actually prefers to feed on flowers of three Brassica nigra genotypes rather than on their leaves. First- and second-instar caterpillars were observed to feed primarily on leaves, whereas late second and early third instars migrated via the small leaves of the flower branches to the flower buds and flowers. Once flower feeding began, no further leaf feeding was observed. We investigated growth rates of caterpillars having access exclusively to either leaves of flowering plants or flowers. In addition, we analyzed glucosinolate concentrations in leaves and flowers. Late-second- and early-third-instar P. brassicae caterpillars moved upward into the inflorescences of B. nigra and fed on buds and flowers until the end of the final (fifth) instar, after which they entered into the wandering stage, leaving the plant in search of a pupation site. Flower feeding sustained a significantly higher growth rate than leaf feeding. Flowers contained levels of glucosinolates up to five times higher than those of leaves. Five glucosinolates were identified: the aliphatic sinigrin, the aromatic phenyethylglucosinolate, and three indole glucosinolates: glucobrassicin, 4-methoxyglucobrassicin, and 4-hydroxyglucobrassicin. Tissue type and genotype were the most important factors affecting levels of identified glucosinolates. Sinigrin was by far the most abundant compound in all three genotypes. Sinigrin, 4-hydroxyglucobrassicin, and phenylethylglucosinolate were present at significantly higher levels in flowers than in leaves. In response to caterpillar feeding, sinigrin levels in both leaves and flowers were significantly higher than in undamaged plants, whereas 4-hydroxyglucobrassicin leaf levels were lower. Our results show that feeding on flower tissues, containing higher concentrations of glucosinolates, provides P. brassicae with a nutritional benefit in terms of higher growth rate. This preference appears to be in contrast to published negative effects of volatile glucosinolate breakdown products on the closely related Pieris rapae.     

Synergism between myristicin and xanthotoxin,a naturally cooccurring plant toxicant

Myristicin, a methylenedioxyphenyl (MDP)-containing phenylpropene constituent of the leaves of many plants in the family Umbelliferae, is a highly effective Synergist of the cooccurring furanocoumarin xanthotoxin. As little as 0.10 % in an artificial diet can increase the toxicity of xanthotoxin toHeliothis zea (Lepidotera: Noctuidae) fivefold. In addition to increasing the proportion of caterpillars dying at a given xanthotoxin concentration, myristicin also increases the rate at which they die and increases the time to molt of surviving larvae. That there was no increase in the deterrency of xanthotoxin in the presence of myristicin suggests that the mechanism of synergism is not behaviorial but rather is biochemical, via MDP competitive inhibition of microsomal mixed function oxidases.     

Neonate Silkworm (<Emphasis Type="Italic">Bombyx mori</Emphasis>) Larvae Are Attracted to Mulberry (<Emphasis Type="Italic">Morus alba</Emphasis>) Leaves with Conspecific Feeding Damage

The silkworm Bombyx mori is a molecular genetic model for the Lepidoptera. Its odorant receptor genes have been described, and preliminary studies suggest that several are expressed specifically in the larval caterpillar stage. This study was undertaken to identify olfactory behaviors specific to the larvae. A two-choice leaf disk bioassay with naive neonate larvae was used to evaluate the attractiveness of three types of mulberry leaf (Morus alba): newly flushed leaves from branch tips, mature leaves, and mature leaves with feeding damage caused by conspecific larvae. Mature leaves with feeding damage were the most attractive, newly flushed leaves were moderately favored, and undamaged mature leaves were the least attractive. Volatile odors collected from whole mulberry leaves by using solid-phase microextraction fibers were analyzed by gas chromatography-mass spectrometry. The volatile profile of newly flushed leaves and mature leaves damaged by conspecific larvae was more complex compared to undamaged mature leaves. By comparing the volatile makeup of each leaf type, a list of 22 candidate odors responsible for attracting the neonate larvae was generated; α-farnesene was particularly notable as a herbivore-induced volatile. These odors will be used in future in vitro studies to determine whether they activate larval-specific odorant receptors. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Jasmonic Acid-Induced Changes in <Emphasis Type="BoldItalic">Brassica oleracea</Emphasis> Affect Oviposition Preference of Two Specialist Herbivores

Jasmonic acid (JA) is a key hormone involved in plant defense responses. The effect of JA treatment of cabbage plants on their acceptability for oviposition by two species of cabbage white butterflies, Pieris rapae and P. brassicae, was investigated. Both butterfly species laid fewer eggs on leaves of JA-treated plants compared to control plants. We show that this is due to processes in the plant after JA treatment rather than an effect of JA itself. The oviposition preference for control plants is adaptive, as development time from larval hatch until pupation of P. rapae caterpillars was longer on JA-treated plants. Total glucosinolate content in leaf surface extracts was similar for control and treated plants; however, two of the five glucosinolates were present in lower amounts in leaf surface extracts of JA-treated plants. When the butterflies were offered a choice between the purified glucosinolate fraction isolated from leaf surface extracts of JA-treated plants and that from control plants, they did not discriminate. Changes in leaf surface glucosinolate profile, therefore, do not seem to explain the change in oviposition preference of the butterflies after JA treatment, suggesting that as yet unknown infochemicals are involved.     

Changes in leaf mono- and sesquiterpene metabolism with nitrate availability and leaf age inHeterotheca subaxillaris

The concentration of leaf mono- and sesquiterpenes is greater in nitrate-limited than in nitrate-richHeterotheca subaxillaris plants and is highest in young leaves and declines with leaf age. To determine whether rates of volatile terpene synthesis and/or loss vary with nitrate availability and leaf age, incorporation of¹⁴C from photosynthetically fixed¹⁴CO₂ and the subsequent loss of label was measured in plants grown under nitrate-limited and nitrate-rich conditions.¹⁴C incorporation into mono- and sesquiterpenes was greater in nitrate-limited than in nitrate-rich plants and was highest in young leaves and declined with leaf age. Incorporation continued for several days after exposure, while loss of label was slow until leaves were 4–6 weeks old. These results suggest that the higher leaf volatile terpene content observed under nitrate limitation apparently results from increased synthesis per leaf and accumulation of mono- and sesquiterpenes in immature leaves of nitratepoor plants. Furthermore, volatile terpene synthesis is highest in young leaves, declines with leaf age, and is very low in older leaves. Carbon used for synthesis of this pool may be derived from both current photosynthesis as well as carbon transported to young leaves from older leaves. These data are consistent with hypotheses that predict that greater levels of carbon-based chemical defenses occur in plants under nutrient limitation. The apparent low metabolic cost of maintenance (i.e., slow turnover) of the accumulated terpenoid pool would limit the energetic cost of volatile terpenes as a chemical defense.     

Relationship between nutritional composition of plant species and infestation levels of thrips

Levels of soluble protein and carbohydrate (raffinose, sucrose, glucose, and fructose) in leaves from a selection of plant species were measured to determine if a relationship existed between these nutrients and infestation by Frankliniella occidentalis and Heliothrips haemorrhoidalis. Most species of host plant examined contained a higher proportion of protein than carbohydrates, and overall, leaves from species of plants that supported populations of thrips had greater levels of protein than leaves from nonhost species. New leaves and flowers that supported F. occidentalis contained high levels of carbohydrate and protein. The quantity of protein in leaves at the top of the tree, Peumus boldus, was greater than in leaves from lower levels, and the amount of feeding damage accrued by H. haemorrhoidalis was greater on the upper foliage than lower foliage. Oviposition by H. haemorrhoidalis was positively correlated to levels of protein in host plants but not to levels of carbohydrates. Overall, levels of soluble protein in plants influenced their susceptibility to thrips more than levels of carbohydrates.