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Oviposition responses after prior feeding by P. rapae larvae. Oviposition choice tests comparing Col-0 ( n 5 12) and cyp79B2 cyp79B3 ( n 5 20) plants with and without prior feeding by two third- instar P. rapae larvae for 3 h. Mean 6 SE , comparisons for significance
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Like many crucifer-specialist herbivores, Pieris rapae uses the presence of glucosinolates as a signal for oviposition and larval feeding. Arabidopsis thaliana glucosinolate-related mutants provide a unique resource for studying the in vivo role of these compounds in affecting P. rapae oviposition. Low indole glucosinolate cyp79B2 cyp79B3 mutants r...
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Context 1
... of glucosinolate biology (Kliebenstein et al., 2001; Lambrix et al., 2001), we used transgenic Col-0 overexpressing ESP from the cauliflower mosaic virus 35S promoter (35S: ESP ; Burow et al., 2006b) in a more specific assay to study the effects of nitriles on P. rapae oviposition. Compared to empty-vector control plants, surface washes of 35S: ESP plants contained approximately 4-fold more IAN, whereas no significant difference was observed in the abundance of I3C (Fig. 4B). Although the ESP-overexpressing plants with high nitrile levels received significantly fewer P. rapae eggs (Fig. 3E), hatching success and larval weight gain were unaffected (Supplemental Fig. S2, A and B). Therefore, these data suggest that nitrile formation during glucosinolate breakdown can play a significant role in deterring oviposition. ESP modulates glucosinolate breakdown through a direct interaction with myrosinase (Burow et al., 2006a). Therefore, given the clear effects of ESP overproduction (Fig. 3E), it seemed likely that the absence of myrosinase in tgg1 tgg2 mutants (Barth and Jander, 2006) would also influence P. rapae oviposition. Some- what surprisingly, there was no significant difference in the number of eggs deposited on wild-type and tgg1 tgg2 mutant plants (Fig. 3F), even if the plants were mechanically damaged to promote glucosinolate breakdown prior to the oviposition assay (Fig. 3G). Indole glucosinolates in damaged plant tissue un- dergo degradation that is independent of the TGG1 and TGG2 myrosinases (Barth and Jander, 2006). To investigate whether this myrosinase-independent breakdown influences P. rapae oviposition, we performed pair-wise comparisons of oviposition on cyp79B2 cyp79B3 tgg1 tgg2 quadruple mutants with tgg1 tgg2 and cyp79B2 cyp79B3 double mutants. Figure 3H shows that tgg1 tgg2 plants are more attractive than the quadruple mutant, whereas cyp79B2 cyp79B3 were equally attractive (Fig. 3I). This indicates that TGG1 and TGG2-dependent breakdown of indole glucosinolates is not essential for the production of P. rapae oviposition cues. Ovipositing P. rapae females are deterred by ESP activity in the tgg1 tgg2 mutant background (Fig. 3J) but not by plants transformed with an empty vector (EV) control (Fig. 3K). Because the action of ESP depends on the physical interaction with myrosinase (Lambrix et al., 2001; Burow et al., 2006a), this result indicates that some other myrosinase might break down indole glucosinolates in the tgg1 tgg2 mutant background. To test this hypothesis, indole glucosinolate breakdown products were mea- sured in leaf surface washes of tgg1 tgg2 mutants, with and without ESP overexpression. Similar to results obtained for 35S: ESP and EV wild-type plants (Fig. 4B), there was a significantly elevated IAN in surface washes of 35S: ESP tgg1 tgg2 plants and no significant difference in I3C abundance (Fig. 4C). Whereas wild-type Col-0 produces I3C as the primary I3M breakdown product, plants expressing ESP produce primarily IAN (Miao and Zentgraf, 2007; Burow et al., 2008). To determine whether these two metabolites differentially affect P. rapae oviposition, cyp79B2 cyp79B3 plants, which contain low indole glucosinolate levels, were sprayed with IAN and I3C for oviposition experiments. Compared to mock-treated control plants, cyp79B2 cyp79B3 plants treated with 1 m M IAN received fewer eggs (Fig. 5A), indicating that IAN deters oviposition. Because IAN is volatile, the presence of this compound on the leaves during the entire experiment was confirmed with a surface wash of the plants 24 h after treatment (Fig. 5B). IAN deters P. rapae oviposition over a wide range of concentrations, with a 0.01 m M IAN application still having a significant deterrent effect (Fig. 5C). IAN concentration in leaf surface washes of ESP-expressing plants (i.e. L er and 35S: ESP ; Fig. 4, A and B) is within the range of exogenous IAN applications that were tested. In contrast to IAN addition, I3C-treated cyp79B2 cyp79B3 plants received significantly more eggs than wild-type controls, indicating that this indole glucosinolate breakdown product is attractive to female P. rapae (Fig. 5D). I3C was abundant in surface washes 24 h after spraying Arabidopsis plants with 1 m M I3C (Fig. 5E). Because this I3C concentration greatly ex- ceeded that found in surface washes of untreated Col-0 leaves (Fig. 4A), we also tested the oviposition response of P. rapae on leaves that were treated with 100-fold less I3C. Compared to mock-treated leaves, oviposition was higher on cyp79B2 cyp79B3 leaves treated with 0.01 m M I3C (Fig. 4F), showing that, like IAN, I3C functions as an oviposition cue over a wide range of concentrations. It was demonstrated previously that female P. rapae avoid ovipositing on plants infested with conspecific larvae (Rothschild and Schoonhoven, 1977). We observed this phenomenon with wild-type, but not cyp79B2 cyp79B3 mutant, plants (Fig. 6). The deterrent effects of larvae-infested plants (Fig. 6) and exogenous IAN (Fig. 5) suggested that IAN in larval regurgitant or frass could contribute to the avoidance of infested plants by female P. rapae. P. rapae larvae make use of gut-specific nitrile specifier protein to direct breakdown of glucosinolates to nitriles rather than the more toxic isothiocyanates, an adaptation that results in the presence of glucosinolate- derived nitriles in larval frass (Wittstock et al., 2004). Compared to larvae feeding on cyp79B2 cyp79B3 plants, both regurgitant (Fig. 7A) and frass (Fig. 7B) from larvae feeding on Col-0 plants contain significantly higher amounts of IAN. During feeding bouts, lepidopteran larvae typically apply small amounts of regurgitant onto the feeding site (Truitt and Par ́ , 2004). Application of 2 m L fresh regurgitant from Col-0-fed larvae to cyp79B2 cyp79B3 leaves in a detached-leaf assay (Fig. 2B) showed that this regurgitant acts as a significant deterrent for P. rapae oviposition (Fig. 7C). The regurgitant applied to a single leaf (approximately 25 m g cm 2 2 IAN) was comparable to IAN levels detected in surface washes of L er (10.6 m g cm 2 2 IAN) and 35S: ESP (6.4 m g cm 2 2 IAN), or cyp79B2 cyp79B3 plants sprayed with 1 m M IAN (44.2 m g cm 2 2 IAN). A direct comparison of regurgitant from cyp79B2 cyp79B3 fed and Col-0-fed larvae showed that the deterrent effect requires the presence of an indole-derived compound in the host plant tissue (Fig. 7D). Addition of approximately 5 mg of larval frass, which has lower IAN levels than regurgitant (Fig. 7, A and B), to a detached-leaf assay (Fig. 2B) did not have a significant effect on P. rapae oviposition ( cyp79B2 cyp79B3 ...
Context 2
... Because L er and Col-0 plants differ in several as- pects of glucosinolate biology (Kliebenstein et al., 2001; Lambrix et al., 2001), we used transgenic Col-0 overexpressing ESP from the cauliflower mosaic virus 35S promoter (35S: ESP ; Burow et al., 2006b) in a more specific assay to study the effects of nitriles on P. rapae oviposition. Compared to empty-vector control plants, surface washes of 35S: ESP plants contained approximately 4-fold more IAN, whereas no significant difference was observed in the abundance of I3C (Fig. 4B). Although the ESP-overexpressing plants with high nitrile levels received significantly fewer P. rapae eggs (Fig. 3E), hatching success and larval weight gain were unaffected (Supplemental Fig. S2, A and B). Therefore, these data suggest that nitrile formation during glucosinolate breakdown can play a significant role in deterring oviposition. ESP modulates glucosinolate breakdown through a direct interaction with myrosinase (Burow et al., 2006a). Therefore, given the clear effects of ESP overproduction (Fig. 3E), it seemed likely that the absence of myrosinase in tgg1 tgg2 mutants (Barth and Jander, 2006) would also influence P. rapae oviposition. Some- what surprisingly, there was no significant difference in the number of eggs deposited on wild-type and tgg1 tgg2 mutant plants (Fig. 3F), even if the plants were mechanically damaged to promote glucosinolate breakdown prior to the oviposition assay (Fig. 3G). Indole glucosinolates in damaged plant tissue un- dergo degradation that is independent of the TGG1 and TGG2 myrosinases (Barth and Jander, 2006). To investigate whether this myrosinase-independent breakdown influences P. rapae oviposition, we performed pair-wise comparisons of oviposition on cyp79B2 cyp79B3 tgg1 tgg2 quadruple mutants with tgg1 tgg2 and cyp79B2 cyp79B3 double mutants. Figure 3H shows that tgg1 tgg2 plants are more attractive than the quadruple mutant, whereas cyp79B2 cyp79B3 were equally attractive (Fig. 3I). This indicates that TGG1 and TGG2-dependent breakdown of indole glucosinolates is not essential for the production of P. rapae oviposition cues. Ovipositing P. rapae females are deterred by ESP activity in the tgg1 tgg2 mutant background (Fig. 3J) but not by plants transformed with an empty vector (EV) control (Fig. 3K). Because the action of ESP depends on the physical interaction with myrosinase (Lambrix et al., 2001; Burow et al., 2006a), this result indicates that some other myrosinase might break down indole glucosinolates in the tgg1 tgg2 mutant background. To test this hypothesis, indole glucosinolate breakdown products were mea- sured in leaf surface washes of tgg1 tgg2 mutants, with and without ESP overexpression. Similar to results obtained for 35S: ESP and EV wild-type plants (Fig. 4B), there was a significantly elevated IAN in surface washes of 35S: ESP tgg1 tgg2 plants and no significant difference in I3C abundance (Fig. 4C). Whereas wild-type Col-0 produces I3C as the primary I3M breakdown product, plants expressing ESP produce primarily IAN (Miao and Zentgraf, 2007; Burow et al., 2008). To determine whether these two metabolites differentially affect P. rapae oviposition, cyp79B2 cyp79B3 plants, which contain low indole glucosinolate levels, were sprayed with IAN and I3C for oviposition experiments. Compared to mock-treated control plants, cyp79B2 cyp79B3 plants treated with 1 m M IAN received fewer eggs (Fig. 5A), indicating that IAN deters oviposition. Because IAN is volatile, the presence of this compound on the leaves during the entire experiment was confirmed with a surface wash of the plants 24 h after treatment (Fig. 5B). IAN deters P. rapae oviposition over a wide range of concentrations, with a 0.01 m M IAN application still having a significant deterrent effect (Fig. 5C). IAN concentration in leaf surface washes of ESP-expressing plants (i.e. L er and 35S: ESP ; Fig. 4, A and B) is within the range of exogenous IAN applications that were tested. In contrast to IAN addition, I3C-treated cyp79B2 cyp79B3 plants received significantly more eggs than wild-type controls, indicating that this indole glucosinolate breakdown product is attractive to female P. rapae (Fig. 5D). I3C was abundant in surface washes 24 h after spraying Arabidopsis plants with 1 m M I3C (Fig. 5E). Because this I3C concentration greatly ex- ceeded that found in surface washes of untreated Col-0 leaves (Fig. 4A), we also tested the oviposition response of P. rapae on leaves that were treated with 100-fold less I3C. Compared to mock-treated leaves, oviposition was higher on cyp79B2 cyp79B3 leaves treated with 0.01 m M I3C (Fig. 4F), showing that, like IAN, I3C functions as an oviposition cue over a wide range of concentrations. It was demonstrated previously that female P. rapae avoid ovipositing on plants infested with conspecific larvae (Rothschild and Schoonhoven, 1977). We observed this phenomenon with wild-type, but not cyp79B2 cyp79B3 mutant, plants (Fig. 6). The deterrent effects of larvae-infested plants (Fig. 6) and exogenous IAN (Fig. 5) suggested that IAN in larval regurgitant or frass could contribute to the avoidance of infested plants by female P. rapae. P. rapae larvae make use of gut-specific nitrile specifier protein to direct breakdown of glucosinolates to nitriles rather than the more toxic isothiocyanates, an adaptation that results in the presence of glucosinolate- derived nitriles in larval frass (Wittstock et al., 2004). Compared to larvae feeding on cyp79B2 cyp79B3 plants, both regurgitant (Fig. 7A) and frass (Fig. 7B) from larvae feeding on Col-0 plants contain significantly higher amounts of IAN. During feeding bouts, lepidopteran larvae typically apply small amounts of regurgitant onto the feeding site (Truitt and Par ́ , 2004). Application of 2 m L fresh regurgitant from Col-0-fed larvae to cyp79B2 cyp79B3 leaves in a detached-leaf assay (Fig. 2B) showed that this regurgitant acts as a significant deterrent for P. rapae oviposition (Fig. 7C). The regurgitant applied to a single leaf (approximately 25 m g cm 2 2 IAN) was comparable to IAN levels detected in surface washes of L er (10.6 m g cm 2 2 IAN) and 35S: ESP (6.4 m g cm 2 2 IAN), or cyp79B2 cyp79B3 plants sprayed with 1 m M IAN (44.2 m g cm 2 2 IAN). A direct comparison of regurgitant from cyp79B2 cyp79B3 fed and Col-0-fed larvae showed that the deterrent effect requires the presence of an indole-derived compound in the host plant tissue (Fig. 7D). Addition of approximately 5 mg of larval frass, which has lower IAN levels than regurgitant (Fig. 7, A and B), to a detached-leaf assay (Fig. 2B) did not have a significant effect on P. rapae oviposition ( cyp79B2 cyp79B3 ...
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Glucosinolates are plant secondary metabolites that act as direct defenses against insect herbivores and various pathogens. Recent analysis has shown that methionine-derived glucosinolates are hydrolyzed/activated into either nitriles or isothiocyanates depending upon the plants genotype at multiple loci. While it has been hypothesized that tryptop...
The glucosinolate–myrosinase system, found in plants of the order Brassicales, has long been considered an effective defense system against herbivores. The defensive potential of glucosinolates is mainly due to the products formed after myrosinase-catalyzed hydrolysis upon tissue damage. The most prominent hydrolysis products, the isothiocyanates,...
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... Larvae of the small white possess a nitrile-specifier protein that directs glucosinolate hydrolysis to the formation of the less toxic nitriles, which allows them to feed on glucosinolate-containing crucifers (Wittstock et al. 2004;Agerbirk et al. 2010;Jeschke et al. 2016;Mesimeri et al. 2024). Glucosinolates and their glucosinolates products can affect plant resistance to small white larvae (Giamoustaris and Mithen 1995;Agrawal and Kurashige 2003;De Vos et al. 2008;Santolamazza-Carbone et al. 2016;Badenes-Pérez 2023) and can also act as host recognition cues for small white butterflies prior to ovipositing on plants (Renwick et al. 1992;Müller et al. 2010;Badenes-Pérez 2023). When making intraspecific comparison among plant accessions of Arabidosis thaliana L. and Brassica oleracea L. (Brassicaceae) that had different glucosinolate content, small white butterflies preferred to oviposit on accessions with higher total glucosinolate content and lower concentrations of certain aliphatic glucosinolates (Poelman et al. 2009;Müller et al. 2010;Coolen et al. 2022). ...
Several Barbarea spp. (Brassicaceae) have been tested as trap crops for the diamondback moth Plutella xylostella L. (Lepidoptera: Plutellidae). The use of trap crops can be affected by their susceptibility to other pests, especially if the purpose is to reduce insecticide use. Barbarea rupicola Moris, B. verna (Mill.) Asch., and B. vulgaris Aiton (types G and P) (Brassicaceae) were tested for their susceptibility to the cabbage whitefly Aleyrodes proletella L. (Hemiptera: Aleyrodidae). The percentage of plants showing infestation by cabbage whiteflies ranged from 50% in G-type B. vulgaris and 8.3% in B. verna to no infestation at all in B. rupicola and P-type B. vulgaris. On the other hand, 95.8% of P-type plants showed symptoms of powdery mildew, Erysiphe cruciferarum Opiz ex L. Junell (Erysiphales: Erysiphaceae), while the G type and the other Barbarea spp. were unaffected by this pathogen. Additionally, the G and P types were used in two-choice oviposition preference tests to compare their attractiveness to the small white butterfly Pieris rapae L. (Lepidoptera: Pieridae). No significant differences in total oviposition per plant were found between the two types, but within-plant differences show that the small white butterfly prefers to oviposit on the adaxial leaf side in the P type. This study indicates that in locations where the cabbage whitefly is an economic pest, B. verna, which can also be used as a dead-end trap crop for the diamondback moth, could be chosen over G-type B. vulgaris.
... In the pursuit of exploring new antimicrobial drugs, we intended to investigate 3-indoleacetonitrile (3-ICN) (Figure 1), also known as auxin, a plant growth hormone produced by cruciferous vegetables such as broccoli, cabbage, and cauliflower. 28 Several reports have stated that 3-ICN could decrease the ability to form biofilms, hamper motility, and inhibit prodigiosin by interfering with the QS in S. marcescens. 29,30 Nevertheless, highly selective and active novel candidates are in high demand to enable a comprehensive investigation of QS inhibition in S. marcescens. ...
... In the presence of these proteins, the production of isothiocyanates is reduced in favour of other breakdown products, such as simple nitriles, epithionitriles, and organic thiocyanates. This introduces additional structural diversification, besides the biosynthesis process, and may provide further defence mechanisms through direct or indirect effects on plant enemies [134,135]. ...
The ability of plants to release chemicals that affect the growth of other plants offers potential benefits for weed management and sustainable agriculture. This review explores the use of Camelina sativa as a promising cover crop with weed control potential. Camelina sativa, known for its high oil content and adaptability to diverse climatic conditions, exhibits allelopathic potential by releasing chemical compounds that inhibit weed growth. The crop's vigorous growth and canopy architecture contribute to effective weed suppression, reducing the prevalence and spread of associated pathogens. Furthermore, the chemical compounds released by camelina through the solubilization of compounds from leaves by rain, root exudation, or deriving from microbial-mediated decay of camelina's tissues interfere with the growth of neighbouring plants, indicating allelopathic interactions. The isolation and identification of benzylamine and glucosinolates as allelochemicals in camelina highlight their role in plant-plant interactions. However, the studies carried out on this species are outdated, and it cannot be excluded that other chemicals deriving from the breakdown of the glucosinolates or belonging to other classes of specialized metabolites can be involved in its allelopathic potential. Camelina sativa also demonstrates disease suppression capabilities, with glucosinolates exhibiting fungicidal, nematocidal, and bactericidal activities. Additionally, camelina cover crops have been found to reduce root diseases and enhance growth and yields in corn and soybeans. This review sheds light on the allelopathic and agronomic benefits of Camelina sativa, emphasizing its potential as a sustainable and integrated pest management strategy in agriculture.
... So, the underground area requires specific insecticides (indolic GLS) to better protect plants. De Vos et al. [53] found indole-3-acetonitrile (IAN) could reduce laying oviposition on Arabidopsis. The GLS and their hydrolysis products might form thiohydroxamate-O-sulfonates (insect deterrent compounds), as well as toxic nitriles and epithionitriles, facilitating the protection of plants from damage. ...
... Overall, the GLS of the M18-15 were significantly higher than LQ66, except in the roots of I3M which was higher than LQ66, and there was no significant difference between the other three GLS in LQ66 (Figure 10). From a defensive point of view, the 4OH-I3M, 4MOI3M, and NMOI3M are more capable of defending against aphids [51,53], and their root systems maintain maximum ecological adaptation. The future study could focus on the transport process of high-GLS and low-GLS varieties, which will stimulate research on the transport of defensive compounds as well as other metabolites (flavonoids and carotenoids). ...
Cabbage (Brassica oleracea L. var. capitata) is an excellent source of glucosinolates (GLS) that could reduce the risk of chronic diseases. The purpose of this study was to investigate the biological traits, pigment contents, color, and GLS content of 13 cabbage varieties. This study found that there were significant differences in the GLS content for various developmental stages of cabbage varieties, and the accumulation of GLS in young leaves was higher than that in mature stages. In most of the samples, the GLS content accumulated in different parts and changed as inner leaf > middle leaf > condensed stem > root. Double haploids of the M18-15 variety may be good candidates for future breeding programs and consumers, due to their high GLS content (ranging from 201.10 to 396.25 nmol mg−1 FW). GLS also act as a defense substance, and the data related to GLS accumulation patterns in different leaf locations and root parts may be useful for understanding leaf defense mechanisms and potential source–sink relationships. In addition, the observed interspecific variability is beneficial for breeders to develop Brassica varieties with high GLS content, as well as for the development of new functional food additives.
... Different glucosinolates can also stimulate oviposition differently, and P. rapae prefers indol-3-ylmethylglucosinolate and 2-phenylethylglucosinolate over allylglucosinolate [23,27,28]. On the other hand, indole-3acetonitrile, which is derived from indol-3-ylmethylglucosinolate and can be present in the regurgitant of P. rapae larvae, can be an oviposition deterrent [29]. When comparing plants of the same species with different glucosinolate content, P. rapae also preferred to oviposit on lines with higher concentrations of total glucosinolates and lower concentrations of certain aliphatic glucosinolates [10,30,31]. ...
Glucosinolates are used in host-plant recognition by insects specialized on Brassicaceae, such as Pieris rapae L. (Lepidoptera: Pieridae). This research investigated the association between P. rapae oviposition and larval survival and host-plant glucosinolate content using 17 plant species in which glucosinolate content had previously been determined. Two-choice oviposition tests (comparing each plant species to Arabidopsis thaliana L.) and larval survival experiments showed that indolic glucosinolate content had a positive effect on oviposition preference and larval survival in P. rapae. In the host plants tested, the effects of indolic glucosinolates on oviposition preference and of glucosinolate complexity index and aliphatic glucosinolates without sulfur-containing side chains on total oviposition were smaller on P. rapae than on Plutella xylostella L. (Lepidoptera: Plutellidae), another lepidopteran specialized on glucosinolate-containing plants. This study suggests that high indolic glucosinolate content could make crop plants more susceptible to both P. rapae and P. xylostella, but this effect seems to be greater for P. xylostella. Additionally, as some differences in oviposition and larval survival between P. rapae and P. xylostella occurred in some individual plants, it cannot be concluded that bottom-up factors are always similar in these two specialist insects.
... The consumption of indolic I3M can suppress multiple cancers [51,52]; this potential benefit is mainly due to the formation of cell mutagenesis protector I3C as a degradation product of I3M [53]. From a plant defense perspective, NMOI3M has stronger effects against aphids in the Arabidopsis [54,55]. The order of GLS accumulation in tissues of Chinese cabbage was identified as follows: leaf > middle leaf > outer leaf. ...
Orange Chinese cabbage (Brassica rapa L. ssp. pekinensis) is an excellent source of health-promoting nutrients that could reduce the risk of chronic diseases. This study mainly investigated the accumulation patterns of eight lines of orange Chinese cabbage for indolic glucosinolates (GLSs) and pigment content from representative plant organs across multiple developmental stages. The indolic GLSs were highly accumulated at the rosette stage (S2), especially in inner and middle leaves, and the order of indolic GLSs accumulation in non-edible organs was flower > seed > stem > silique. The expression levels of biosynthetic genes in light signaling, MEP, carotenoids, and GLS pathways were consistent with the metabolic accumulation patterns. The results of a principal component analysis show a clear separation of high indolic GLS lines (15S1094 and 18BC6) from low indolic GLS lines (20S530). A negative correlation between the accumulation of indolic GLS and carotenoids was identified in our study. Our work contributes to providing valuable knowledge required to breed, grow, and select orange Chinese cabbage varieties and their eatable organs with higher nutritional value.
... Similarly, P. rapae tarsal receptors allow the perception of non-volatile glucosinolates that are characteristic components of their cruciferous host plants (St€ adler et al., 1995). Conversely, breakdown products of indole glucosinolates, which can indicate prior larval feeding on host plants, act as contact-mediated oviposition deterrents (De Vos et al., 2008). Specialized metabolites from nonhost plants can have similar negative effects on host-plant choice by ovipositing lepidoptera (Kasubuchi et al., 2018;St€ adler et al., 1995). ...
Non-volatile metabolites constitute the bulk of plant biomass. From the perspective of plant-insect interactions, these structurally diverse compounds including nutritious core metabolites and defensive specialized metabolites. In this review, we synthesize current literature on multiple scales of plant-insect interactions mediated by non-volatile metabolites. At the molecular level, functional genetics studies have revealed a large collection of receptors targeting plant non-volatile metabolites in model insect species and agricultural pests. By contrast, examples of plant receptors of insect-derived molecules remain sparse. For insect herbivores, plant non-volatile metabolites function beyond the dichotomy of core metabolite being nutrients and specialized metabolites being defensive compounds. Insect feeding tends to elicit evolutionarily conserved regulation of plant specialized metabolism, whereas its effect on plant core metabolism varies widely based the interacting species. Finally, several recent studies have demonstrated that non-volatile metabolites can mediate tripartite communication on the community scale, facilitated by physical connections established by direct root-to-root communication, parasitic plants, arbuscular mycorrhizae, and the rhizosphere microbiome. Recent advances in both plant and insect molecular biology, will facilitate further research on the role of non-volatile metabolites in mediating plant-insect interactions.
... Pieris caterpillars are adapted to glucosinolates by producing a gut enzyme that diverts formation of the toxic isothiocyanate hydrolytic breakdown products to less toxic nitriles (Wittstock et al., 2004;Okamura et al., 2019). In addition, Pieris butterflies use glucosinolates as specific feeding and oviposition stimulants through gustatory recognition (Van Loon et al., 1992;Städler et al., 1995;De Vos et al., 2008;Mumm et al., 2008;Hopkins et al., 2009;Ali and Agrawal, 2012). ...
... Previously, Kliebenstein et al. (2001) measured aliphatic-and indole-glucosinolate levels in a range of Arabidopsis accessions, 15 of which were also present amongst the 350 accessions tested in this study (Supplementary Table S2). The class of indole-glucosinolates has been associated with enhanced oviposition preference by P. rapae (Huang and Renwick, 1994;De Vos et al., 2008;Müller et al., 2010). Comparing the normalized average number of eggs deposited on these 15 accessions with the aliphatic-and the indole-glucosinolate levels reported by Kliebenstein et al. (2001) revealed a moderate non-significant positive correlation (R=0.45) between egg number and indoleglucosinolate levels, which points in the same direction as previous findings. ...
... Delker, 2005) with diminished AOC protein synthesis (including AOC1 and partially redundant AOC2, 3, and 4; Leon-Reyes et al., 2010;Stenzel et al., 2012) and a WRKY42 T-DNA insertion line (allele knockout, wrky42-1; Niu et al., 2020) were used in oviposition assays together with wild-type Col-0 plants. A MYC triple-mutant (myc234;Fernandez-Calvo et al., 2011), lacking glucosinolates and affected in JA responsiveness, was taken along as negative control since selection of a suitable brassicaceous host plants by Pieris butterflies occurs via gustatory sensing of glucosinolates (De Vos et al., 2008;Mumm et al., 2008;Hopkins et al., 2009;Ali and Agrawal, 2012;Schweizer et al., 2013). As a control for the effect of JA-dependent plant defenses upstream of AOC1 in the JA-biosynthesis pathway, ALLENE OXIDASE SYNTHASE (AOS) mutant plants (i.e. ...
Insect herbivores are amongst the most destructive plant pests, damaging both naturally occurring and domesticated plants. As sessile organisms, plants make use of structural and chemical barriers to counteract herbivores. However, over 75 percent of herbivorous insect species are well adapted to their host’s defenses and these specialists are generally difficult to ward off. By actively antagonizing the number of insect eggs deposited on plants, future damage by the herbivore’s offspring can be limited. Therefore, it is important to understand which plant traits influence attractiveness for oviposition, especially for specialist insects that are well adapted to their host plants. In this study, we investigated the oviposition preference of Pieris butterflies (Lepidoptera: Pieridae) by offering them the choice between 350 different naturally occurring Arabidopsis thaliana accessions. Using a genome-wide association study of the oviposition data and subsequent fine mapping with full genome sequences of 164 accessions, we identified WRKY42 and AOC1 as candidate genes that are associated with the oviposition preference observed for Pieris butterflies. Host plant choice assays with A. thaliana genotypes impaired in WRKY42 or AOC1 function confirmed a clear role for WRKY42 in oviposition preference of female Pieris butterflies, while for AOC1 the effect was mild. In contrast, WRKY42-impaired plants, that were preferred for oviposition by butterflies, negatively impacted offspring performance. These findings exemplify that plant genotype can have opposite effects on oviposition preference and caterpillar performance. This knowledge can be used for breeding trap crops or crops that are unattractive for oviposition by pest insects.
... For example, methyl salicylate (MeSA), indole-3-acetonitrile or E-2-hexenyl acetate inhibit oviposition, although their respective chemosensory receptors are unknown. [18][19][20] In Arabidopsis, we found that Pieris brassicae butterflies laid fewer eggs on plants pretreated with egg extract, but that this effect was kept in the MeSA biosynthesis mutant bsmt1-1, suggesting that other, yet unknown, compounds repel ovipositing females. [21] However, plants overexpressing BSMT1 or placed next to a MeSA dispenser were still repellent to butterflies. ...
Insect eggs deposited on plants constitute a threat that has led to the evolution of sophisticated defenses. The interactions between insect eggs and plants are governed by a diverse variety of chemicals that inform butterflies about suitable hosts, repel gravid females, alert plants about the presence of an egg, act as signal molecules to induce defenses, directly impair egg development, and indirectly attract egg parasitoids. In recent years, significant progress has been made on the chemical identification, perception and role of compounds associated with oviposition. Knowledge on the genetic basis of oviposition-induced responses is also accumulating. An emerging theme is that insect eggs are not passive structures on leaves but induce complex responses that result from million years of coevolution.
... 55 The prolonged exposure to isothiocyanates causes overall growth retardation in insects. 56 We and others have observed the negative impact on P. xylostella growth and reproduction after hindering the GSSs. 30,32 The response of lepidopterans to isothiocyanates further depends on the class of glucosinolates. ...
The glucosinolate-myrosinase system is a two-component defense system characteristic of cruciferous plants. To evade the glucosinolate-myrosinase system, the crucifer specialist insect, Plutella xylostella, promptly desulfates the glucosinolates into harmless compounds by glucosinolate sulfatases (GSSs) in the gut. In this study, we identified an effective inhibitor of GSSs by virtual screening, molecular docking analysis, and in vitro enzyme inhibition assay. The combined effect of the GSS inhibitor with the plant glucosinolate-myrosinase system was assessed by the bioassay of P. xylostella. We show that irosustat is a GSS inhibitor and the inhibition of GSSs impairs the ability of P. xylostella to detoxify the glucosinolate-myrosinase system, leading to the systematic accumulation of toxic isothiocyanates in larvae, thereby severely affecting feeding, growth, survival, and reproduction of P. xylostella. While fed on the Arabidopsis mutants deficient in myrosinase or glucosinolates, irosustat had no significant negative effect on P. xylostella. These findings reveal that the GSS inhibitor is a novel friendly insecticide to control P. xylostella utilizing the plant glucosinolate-myrosinase system and promote the development of insecticide-plant chemical defense combination strategies.
